horticultural reviews (janick/horticultural) || apple trees: morphology and anatomy

6

Apple Trees: Morphology and Anatomy Charlotte Pratt*

Department of Horticultural Sciences New York State Agricultural Experiment Station Geneva, New York 14456

I. 11.

111.

IV.

V.

VI *

VII. VIII.

IX.

Introduction 265 Seedlings 266 A. Diploid 266 B. Haploid 269 Roots 269 A. Root System 269 B. Primary Body 269 C. Secondary Body 271 Stems 272 A. Shoot System 272 B. Primary Body 274 C. Secondary Body 277 Leaves 283 A. Ontogeny 283 B. Maturity 285 C. Growth rates 287 Vegetative Propagation 288 A. Adventitious Roots 288 B. Adventitious Shoots 289 C. Grafting 290 Size-Controlling Rootstocks 295 Compact or Spur Mutants 297 Concluding Remarks 298 Literature Cited 298

I. INTRODUCTION

A commercial apple tree is a composite, woody, perennial plant. The aerial fruiting portion develops from a bud or stem piece (scion) of a cultivar. There is sometimes an interstem between the scion and the rootstock. The underground portion is a rooted stem, or root piece, of a clon- ally or seed-propagated rootstock. The rootstock produces adventitious

'I thank M. C. Goffinet and A. N. Lakso for their help in the preparation of the figures.

265

Horticultural Reviews Edited by Jules Janiek

Copyright © 1990 Timber Press, Inc.

CHARLOTTE PRATT 266

feeding and anchoring roots, and influences the size and fruiting precocity of the scion.

The previous review (Pratt 1988) related chronologically the formation of apple fruit buds, inflorescences, flowers, seeds, and fruits. The present review continues the story, beginning with the structure of the mature embryo and the young seedling. It then examines the development of roots, stems, and leaves in an apple tree. It takes up the morphology and anatomy of vegetative propagation of apple plants. It concludes with a brief discussion of size-controlling rootstocks and of compact or spur mutants. In vitro propagation is not included.

The standard for literature cited is similar to that used in the companion review (Pratt 1988). For each topic only the most recent funda- mental papers are selected. This means that the cited literature is not an exhaustive bibliography; the indicated papers must often be consulted for additional references.

Wherever necessary, studies on closely related species, especially pear, are used to round out the morphological and anatomical picture. Further research is needed to establish the validity of these accounts for apple. Sometimes secondary sources, such as those by Eames and MacDaniels (19471, Esau (1965, 19771, and Koslowski (19711, are cited to interpret the relevance of certain anatomical events to the life of the tree. Eames and MacDaniels (1947) is the best reference for morphology and anatomy of apple, partly because it embodies many observations by L. H. MacDaniels not published elsewhere. Published papers and unpub- lished theses through 1988 in English, French, or German, with only a few personal communications, are cited. Papers in other languages have been read in translated abstracts.

Since this review incorporates both botanical and horticultural literature, Soule’s (1985) glossary is the most appropriate reference for terminology. Botanical terms not readily located in Soule’s glossary may be found in Eames and MacDaniels (19471, Esau (1965, 19771, Metcalfe and Chalk (19501, and Solereder (1908). I have defined specialized or proposed terminology in the text.

Malus X domestica Borkh. is used as the scientific name of the cultivated apple (Korban and Skirvin 1984). The nomenclature of other Malus species is that used by the Liberty Hyde Bailey Hortorium (1976).

11. SEEDLINGS

A. Diploid

An apple embryo has a hypocotyl-root axis bearing 2, rarely 3, cotyledons, a flat epicotyl or plumule, and the radicle (Esau 1965; Pratt 1988; Way et al. 1976). At germination the epicotyl has produced 3 leaf primordia (Way et al. 1976). It elongates so that the seed is elevated above

6. APPLE TREES: MORPHOLOGY AND ANATOMY 267

the soil. The testa splits and is shed as the cotyledons expand. The young seedling apical meristem lacks cuticle, has two tunica layers, a corpus with a short pith rib meristem grading into a ribbed, vacuolated pith. By one month after germination, an average of 4 spirally arranged leaves have expanded, and 4 more leaves are developing in the terminal bud.

The seedling tap root (Way et al. 1976) has exarch, usually tetrarch, primary xylem (Stoutemyer 1937) (Fig. 6.1). The so-called endodermis has large casparian strips, which were thought by MacKenzie (1979) to have been phi thickenings. The true endodermis lies between the phi layer and the pericycle. The pericycle, where lateral roots originate, is 1- 2 cells thick. The cortex is shed gradually but early in the life of the root, and it is replaced by phellogen originating in the pericycle (Stoutemyer 1937). The resulting periderm is brown, cells thick-walled, densely cytoplasmic, and stratified. Seedling root anatomy was also studied by Riedhart and Guard (1957), Siegler and Bowman (19391, and Weerden- berg and Peterson (1983) (see Roots).

The change from the radial organization of primary vascular tissues in the root to the collateral vascular bundles of the stem occurs in the hypocotyl between the cotyledonarynode and the root (Esau 1965). It was unfortunately not studied by Stoutemyer (1937).

Fig. 6.1. Young tetrarch primary root of apple sectioned transversely to show cortex with phi layer and endodermis, and protostele with two layers of pericycle and alternate poles of protophloem (sieve element) and protoxylem (tracheid). Metaxylem in center has not yet differentiated. X600. (Siegler and Bowman 1939).

268 CHARLOTTE PRATT

Seedling stems have about 5 procambial strands, and enda'rch primary xylem (Stoutemyer 1937). Phellogen usually originates from periclinal divisions in the epidermis.

Older seedlings have smoother, less hairy bark with more prominent lenticels than mature stems (Fritzsche 1948). Seedling stems are also more rigid, because they have more secondary xylem than bark and pith, fewer vessels and axial and ray parenchyma cells, and more fibers than mature stems. The first growth ring of a seedling has these anatomical characteristics, whereas subsequent rings are considered more mature, because they have a large number of vessels, especially in the late wood of each ring. Seedling apple leaves are smaller and thinner than leaves of mature plants (Fritzsche 1948; Stoutemyer 1937; Wuttke 1968; Zimmerman 1972).

In apple seedlings more than a year old, lateral branches from the basal, still juvenile, portion are spreading (at right angles to the main axis) rather than ascending, as in the apical (mature) portion (Fritzsche 1948; Visser 1965). These basal spurs bear a rosette of small leaves, and a small, slender terminal bud which may lose its leaf-like appendages and develop into a thorn (Blair et al. 1956; Fritzsche 1948). Aubertot reported in 1910 that thorny branches of woody rosaceous plants have reduced vascular tissues, including fewer phloem fibers, and sclerified pith forming the point of the thorn. Steps in the inactivation of the apical meristem of the future thorny branch were not mentioned by any of these workers.

The juvenile period is defined by Hackett (1985) as that period (4-8 years after seed germination) in the development of an apple seedling in which flowering does not occur. This is associated with other morphological characteristics, especially the readiness of stems to produce adventitious roots. Zimmerman (1976) found that the number of nodes to first flowering was a better measurement of change to the mature phase than stem height. Node number is related to leaf initiation on the apical meristem, whereas height is dependent on the activity of the sub- apical meristem, which controls internode length [see also Stem, Primary Body).

Some juvenile tissues seem to be still present in apple trees after the juvenile phase. Some juvenile characteristics occur in adventitious shoots from roots of young, nonflowering apple trees, but the stems root less readily than young seedling shoots (Robinson 1975). Juvenile characteristics also occur in shoots from the base of a seedling tree, but not in shoots from the bearing portion of such a tree (Wuttke 1968).

In summary, juvenility is defined as a stage in the development of apple seedlings when stem cuttings most readily form adventitious roots, and before flowering is initiated. It is associated with the above morphological characteristics and lasts an average of 7.5 years (Visser 1964).


B. Haploid The stem structure of a haploid apple clone, selected as a seedling from

a progeny of ‘Topred Delicious’ (Lespinasse and Godicheau 1979), was compared by Lespinasse and Noiton (1986) with the stem anatomy of diploid, triploid, and tetraploid (Dermen 1955) clones of ‘Delicious’. The haploid clone grew more slowly and was smaller in diameter. Its cortex was more sinuous and thicker. The cells of the secondary phloem and xylem were smaller, and the poles of the primary xylem were more irregular than in the other clones, which were similar to each other (Lespinasse and Noiton 1986). The haploid had shorter internodes, shorter, narrower and more pointed leaves, and denser and smaller stomates than did the other clones.

When the haploid clone was whip-and-tongue-grafted onto a diploid ‘Delicious’ rootstock, the very small diameter and slower rate of cell division of the scion retarded, but did not prevent, healing (Noiton et al. 1986). Grafts of diploid ‘Delicious’ on diploid ‘Delicious’, or of tetraploid ‘Delicious’ on diploid ‘Delicious’ involved scions and stocks of similar diameter, and they healed faster. Differences in ploidy did not cause incompatibility. A dwarfing stock, M.9, was a more successful slender stock for the haploid.

111. ROOTS

A. Root System An apple tree has a shallow, horizontal scaffold of adventitious roots

with vertical sinkers (Atkinson 1980; Rogers and Booth 1959), whose horizontal extent is greater than the spread of the branches. Both extent and depth of roots are limited by soil characteristics and tree planting density.

A bimodal curve of primary root growth has a peak coinciding with a peak of shoot growth, and a lesser peak after shoot growth has ended, in England (Atkinson 1980) and in Australia (Cripps 1970).

Death of old roots at the time of transplanting was reported by Barker (1921), but denied by Cripps (1970). The latter found that new roots emerged from the callus at the cut ends of old roots, contrary to the observations of Nightingale (1935) on root grafts.

B. Primary Body The external morphology of new, white, adventitious roots was

described and illustrated by Atkinson (1980), Blanke (1986), and Rogers and Booth (1959). The root hair zone is 1.4 mm, and the maturation zone 2 mm, behind the tip (Blanke 19861. Root hairs are short (0.0254.05 mm

270 CHARLOTTE PRATT

long) (Atkinson 1980); they exude droplets of colorless fluid whose origin and function are unknown. In the maturation zone few root hairs remain, the epidermis is plate-like and corky, and the primary vascular tissue is differentiating (Blanke 1986).

The root cap consists of nearly isodiametric, living cells (Riedhart and Guard 1957). Cortical cells adjacent to the protostele divide periclinally. The inner daughter cells become the endodermis, characterized by casparian strips composed of lignin and suberin on the radial and transverse walls (Atkinson 1980; MacKenzie 1979; Powers and Guard 1950). The outer daughter cells differentiate into the exodermis or inner cortical sheath in pear roots (Esau 19431, or the phi layer in apple roots (Atkinson 1980; MacKenzie 1979; Weerdenburg and Peterson 1983). These cells are characterized by prominent, lignified phi thickenings on the radial walls (Fig. 6.1). The phi layer, function unknown, is peculiar to rosaceous (Solereder 1908) and some other plants. MacKenzie (1979) concluded that the phi layer was misinterpreted as endodermis by Nightingale (1935) and Stoutemyer (1937). I extend this conclusion to the description by Siegler and Bowman (1939) (Fig. 6.1). Powers and Guard (1950) and Riedhart and Guard (1957) mentioned a cortical layer with lignified thickenings, which are presumably phi thickenings, outside the endodermis.

The pericycle was considered part of the protostele of the pear root by Esau (1943). In young roots, it consists of 1 layer in pear (Esau 1943) and apple roots (Powers and Guard 1950; Riedhart and Guard 1957), or 2 layers of cells (Siegler and Bowman 1939) just outside the procambial tissue. The sites (poles) of the first protophloem elements alternate with those of the first protoxylem elements. There are 2-7, usually 5, poles of each, depending on the diameter of the root (Riedhart and Guard 1957). One sieve element differentiates at each protophloem pole, representing the beginning of the primary phloem. When 3 sieve elements are present, protoxylem tracheids have spiral to scalariform thickenings (Riedhart and Guard 1957). Metaxylem differentiates centripetally from the first protoxylem elements to fill the center of the root, and eventually consists of vessels, tracheids, fibers, and parenchyma cells.

After protoxylem differentiates in pear roots, pericycle cells divide periclinally several times (Esau 1943). Lateral (secondary) root primordia originate in the pericycle opposite the protoxylem poles of apple roots (Riedhart and Guard 1957; Siegler and Bowman 1939). A lateral root primordium differentiates a root cap, an apical meristem, and primary root tissues. As the root primordium grows toward the outside of the apple root, phi thickenings disappear from the cortical cells in its path (Weerdenberg and Peterson 1983). At the base of emerging lateral pear roots is a “collar,” which may be misidentified as a lenticel (Esau 1943).

When an apple root is 1-4 weeks old (Atkinson 1980), or at a point 100- 150 mm from the tip (MacKenzie 1979), it turns brown as a result of the death and shedding of the cortex. The dry weight of the cortex is about


equal to that of the stele at the time of shedding (Rogers 1968). Loss of cortex occurs after the lateral roots develop and before the vascular cambium becomes active (Atkinson 1980; MacKenzie 1979). At this stage, many roots, especially lateral roots, die (Atkinson 1980; Rogers 1968). After the cortex is shed, the outerpericycle cells suberize and act as a temporary protective tissue in pear and apple roots (Esau 1943; Stoutemyer 1937). Surviving roots appear brown, and have developed secondary vascular tissues, andlor are invaded by endogenous mycorrhizae (Atkinson 1980).

C. Secondary Body The vascular cambium begins as periclinal cell divisions on the inner

sides of the primary phloem bundles, and becomes continuous a s a result of periclinal divisions in the pericycle outside the primary xylem poles (Fig. 6.2). The cells of the vascular cambium originating from the primary phloem are fusiform initials, and those originating from the pericycle are ray initials. As the cambium produces secondaryphloem cells toward the outside and secondary xylem cells toward the inside, it gradually becomes a continuous cylinder in pear and apple roots (Esau 1943; Ried- hart and Guard 1957).

The secondary xylem of pear roots is composed of vessels, tracheids, fibers, and axial and ray parenchyma (Esau 1943). The rays are of 2 types-the multiseriate, medullary rays originating from ray initials, and the narrow rays originating from divisions in fusiform initials. Secondary phloem consists of blocks of sieve elements, companion cells,

Fig. 6.2. Development of secondary vascular tissues in roots, shown by diagrammatic transverse sections. A. Alternating poles of protophloem (finely stippled] and protoxylem (lightly cross-hatched]; metaxylem not yet differentiated; vascular cambium (dotted lines] on the inner edge of protophloem bundles. B. Vascular cambium (heavy line] has produced secondary phloem and xylem; protophloem is collapsing, metaxylem is lightly cross- hatched. C. Vascular cambium is producing secondary phloem (stippled) on the outside and secondary xylem [finely cross-hatched) on the inside: protophloem has degenerated further. D. Vascular cambium has become symmetrical; protophloem has disappeared: cortex is being lost. Band of parenchyma shown between primary and secondary xylem is absent in apple roots. Loss of cortex occurs in apple roots before stage B. (Eames and MacDaniels 1947).

272 CHARLOTTE PRATT

parenchyma, and fibers separated by rays. The outer limit of the phloem is determined by primary phloem fibers. Sieve elements soon become nonfunctional and partly crushed: phloem parenchyma cells are large. A phellogen develops in the deeper layers of the pericycle, and forms periderm on the permanent roots by the end of the first growing season.

In the second growing season, resumption of secondary growth in surviving apple roots begins independently of the stem, and later in the spring (Knight 1961). Once secondary activity starts, it proceeds from the base of the root towards its white, meristematic tip. New white tips develop on laterals on permanent roots. New adventitious roots develop from the base of the stem of young trees.

Secondary xylem and phloem of the root in woody plants resemble those of the stem. Since they both develop from similar vascular cambia, the differences are “of a quantitative rather than a qualitative kind” (Esau 1965). The differences in vascular tissues between apple stems and roots were experimentally shown to be related to the ground level (Beakbane 1941). Compared to an aerial stem, a buried root had fewer phloem and xylem fibers, fewer and wider vessels, more xylem parenchyma, and thicker bark composed of all the extra-cambial tissues (secondary phloem and periderm). Secondary vessels of apple have bordered pits on the side walls and porous end walls (Eames and MacDaniels 1947). In the apple rootstock M.16, 2% of the end walls had transverse, reticulate to scalariform perforation plates (McKenzie 196lb). Growth rings in permanent apple roots are apparently marked by smaller cells (Beakbane et al. 1941), and they seem less well defined than in the stem.

IV. STEMS

A. Shoot System

The shoot system of an apple tree consists of long (extension) shoots and short shoots (spurs or bourses] (Fig. 6.3) (Abbott 1984: Bijhouwer 1924; Bland 1978; Pratt et al. 1959). In year one, a long shoot bears about 7 bud scales, 9-10 biennial leaves (initiated and partly developed in the previous season and overwintering in the dormant terminal bud), 5-6 annual leaves (developing entirely in year one), and a terminal vegetative or mixed bud (Bland 1978). In year 2 some of the lateral buds on the long shoot develop into dwarf (short) shoots bearing about 8-9 bud scales, a rosette of 9-10 biennial leaves, and a flower cluster, or a terminal vegetative bud (Abbott 1977; Bland 1978; Pratt 1988). A flowering spur develops one or more axillary shoots (bourse shoots) whose terminal meristems may develop into vegetative or mixed buds, which may develop into long or short shoots in the same or later seasons (Abbott 1984).

The differences between leaves of long vs. short shoots are evident


Long Shoot

t Bud Scale Scar X S h o o t Apex

-Foliage L e a f q B u d Scola

D w a r f Shoot gefotive , Tarminates in Flowering Bud

Fig. 6.3. Shoot system of ‘McIntosh’ apple diagrammed for 4 representative years (1970- 1973). On the left, the long (extension] shoot of 1971 had 7 bud scale scars and 10 biennial leaves (present in the overwintering terminal bud of 1970); 6 annual leaves and a terminal vegetative bud were produced during the growing season of 1971; the terminal bud will produce a vegetative short (dwarf) shoot (spur] in 1972. On the right, the dwarf flowering shoot (spur] of 1970 had an axillary (bourse) bud, which developed in 1971 into a vegetative short shoot with 9 bud scales, 10 biennial leaves and a terminal flower bud. This will be a flowering short shoot in 1972; its axillary(bourse] shoot will develop further in 1973. (Bland 1978).

shortly after bud opening (MacDaniels and Cowart 1944). According to their terminology, in the “delayed dormant” stage, bud scales and scale- like leaves abscise. In the stages of “cluster bud,” “pre-pink bud,” and “vegetative spurs,” the small basal spur leaves, which were flat in the dormant bud, expand, and younger leaves have inrolled edges indicating

274 CHARLOTTE PRATT

active cell division in the marginal meristems. In “full pink’; buds, biennial leaves are full size, and the deciduous stipules have not yet fallen. A “terminal vegetative shoot” (long shoot) initiates annual leaves.

The differences in length between mature long shoots and vegetative short shoots were explored in an elaborate, statistical study by Bland (1978). He examined the pith of comparable internodes belonging to biennial leaves in long shoots vs. short shoots, and comparable internodes between annual leaves in long shoots vs. those of bud scales of short shoots. He concluded that long shoots have longer, but not more, internodes than short shoots. The length of an internode depends on the rate and duration of cell division rather than on the length of pith cells.

A vigorous flowering spur usually has 8 leaves in 318 phyllotaxy below the flower cluster (Colby 1934). If more than 8 leaves are present, the internode distal to the eighth leaf elongates, and fruit set is less likely to occur. If 10 leaves are present, phyllotaxy is 2/5, as in long shoots. Colby states that flowering spurs with “small numbers” of leaves rarely fruit. Does this mean less than 8 leaves? The possible relationships between the number and phyllotaxy of spur leaves and fruit set have not yet been explored further.

Bijhouwer (1924) divided long shoots into 3 categories: (1) woodshoots with lateral leaf buds, often terminating in a mixed bud; (2) sylleptic axillary shoots, producing 1-2 leaves early in the same season in which they are formed, and ending in a dormant vegetative bud; and (3) lammas shoots-vegetative long shoots developing late in the growing season (August) with short internodes and with indumentum.

B. Primary Body The apical meristem of a growing vegetative shoot is generally defined

as that portion of the shoot tip distal to the youngest leaf primordium; in woody rosaceous plants related to Malus (Devadas and Beck 1971; Rouffa and Gunckel1951a), the tip of the youngest leaf primordium and the tip of the vegetative apical meristem are at the same level. The latter has 1-3 tunica (T) layers (Blaser and Einset 1948; Dermen 1948; Devadas and Beck 1971; Pratt 1963; Rouffa and Gunckel 1951b), or a variable number of T layers (Rouffa and Gunckel1951a) (Fig. 6.4). The size of an apical meristem changes during leaf initiation and development, but little change occurs in the number of T layers (Rouffa and Gunckel1951b). The cells of the central zone of tunica and corpus stain more lightly than do those of the flanks.

Devadas and Beck (1971) observed residual meristem immediately proximal to the apical meristem. Residual meristem becomes distinct by the vacuolation of cortical and pith cells. Procambial (provascular) leaf traces and interfascicular parenchyma (future medullary rays) differentiate from residual meristem.


lrpus

Fig. 6.4. Apical meristem of Malus sargentii Rehd. in median longitudinal section, showing %layered tunica, corpus, pith rib meristem, and pith. A leaf primordium is being initiated by periclinally divided cells in T-2. Because the files of cells in the pith rib meristem are short and rather irregular, this meristem probably will produce a short shoot (spur). X260. (Rouffa and Gunckel 1951a).

Pith rib meristem originates at the base of the corpus: in a long shoot its cells divide periclinally to form vertical files of cells: in a short shoot (spur) its cells divide for a shorter period and their derivatives are randomly arranged (Rouffa and Gunckel 1951b) (Fig. 6.4). Apple pith is heterogeneous (Solereder 1908), i.e., the peripheral cells of the pith are small living cells with thick walls, while the central cells include both such living cells, which frequently contain tannins, and large, dead, thin- walled cells. Pith cells may contain crystals (Metcalfe and Chalk 1950) and chloroplasts (Swingle 1927). Pith persists for the life of woody stems.

The flanks of the apical meristem give rise to epidermis, cortex, and leaf primordia (see Leaves). The epidermis has hairs (trichomes) and stomates (Schwertfeger and Buchloh 1968). The outer cortex (hypodermis) is composed of thick-walled cells, but the inner cortex has thin-walled cells and intercellular spaces.

The ontogeny of stem vascular tissues is related chronologically and spatially to that of leaves (see Leaves). The emphasis here is on the axial vascular tissues, an arbitrary division of concomitant developmental events.

Procambium and primary phloem develop acropetally in the stem and leaf. Protophloem sieve elements and companion cells are obliterated as metaphloem matures (Devadas and Beck 1971). Both are soon crushed by secondary phloem (Swingle 1927). Primary xylem is initiated in the base of the leaf primordium, differentiating acropetally into the leaf and bidirectionally in the axial bundle in the stem. Protoxylem has spiral tracheids, and metaxylem has radial rows of vessels and tracheids like those of the secondary xylem (Swingle 1927). Protoxylem persists during

276 CHARLOTTE PRATT

the life of a woody stem. Each foliage leaf has an axillary meristem, originally continuous with

the apical meristem, and supplied by 2 bud traces that diverge from the vascular cylinder on either side of the median leaf trace gap: the bud gap is shorter than the leaf gap (Pratt 1967). The first indication of the bud meristem is a shell zone (curving rows of cells) at first on the stem side, and soon afterwards on the leaf side. The shell zone encloses a lenticular central area of irregularly dividing cells. Continued cell division elevates it into a mound, which is continuous with the 2 bud traces. A bud primordium is largest at or just below the leaf axil, and tapers to a double procambial strand which appears in serial transverse sections to end at the top of the median gap. The axillary bud meristem develops into a shoot bearing cataphylls, which eventually become bud scales and transi- tional leaves. When an axillary bud develops into a branch, pith is continuous from the stem through the bud gap into the branch as far as its apical meristem (Fig. 6.5) (MacDaniels 1923).

The primary vascular system was interpreted by Swingle (1927) for apple and by Devadas and Beck (1972) for cherry as composed of stem,

Primary

Secondary phloem J L xylem Cambium L

Fig. 6.5. Node and axillary bud of a 1-year old apple stem in diagrammatic longitudinal section. Bud has several bud scales and leaf primordia with an apical meristem and procambial traces; pith is continuous with the pith of the stem. The median leaf trace of the node traverses the cortex. Periderm and primary and secondary phloem and xylem have developed in the stem; primary xylem is not shown. (Pisek and Eggarter 1959).


leaf, and branch bundles. The latter authors described these relationships as follows: “The leaf trace bundles traverse 5-7 internodes along the stem from the point of their divergence from an axial bundle to the level at which they enter their respective leaf bases. . . , There are about 20 vascular bundles at any given level. One or two of these, depending on the level, are branch traces, five are axial bundles, and the rest are leaf trace bundles.” This statement also summarizes and expands Swingle’s observations.

C. Secondary Body Between the metaphloem and the metaxylem, undifferentiated

meristematic cells divide periclinally to form cambium. Interfascicular parenchyma cells also divide periclinally to become connecting cambium. This continuous cambial cylinder produces annual increments of secondary vascular tissues for the life of that part of the tree. In woody plants generally, cambium develops just before that part of the stem ceases to elongate (Eames and MacDaniels 1947).

At the nodes cambium produces secondary xylem which surrounds and buries leaf and branch traces (Eames and MacDaniels 1947). Leaf traces are ruptured by the lateral pressure of secondary phloem. The proximal parts of the leaf and branch traces persist with the pith and primary xylem. The distal part of the leaf trace is lost when the primary phloem, cortex and early periderm are shed. The distal part of a living branch develops a cambium and secondary vascular tissues of its own, as will be described under crotches. When a branch dies, its base is buried in the secondary xylem as a cone of dead tissue: it is seen as a knot in lumber.

As the vascular cambium develops, epidermal cells divide periclinally (Schwertfeger and Buchloh 1968; Swingle 1927). The inner daughter cells produce a phellogen or cork cambium, which produces several rows of phellem (cork) on the outside and a row of phelloderm cells on the inside (Schwertfeger and Buchloh 1968). The epidermal and phellem cell walls become suberized, forming the periderm. The bases of broken trichomes and lenticels become part of the periderm of a 1-year-old apple stem. The surface of the periderm is smooth with horizontal lenticels (Eames and MacDaniels 1947).

In young, nonflowering trees, starch is present in cortex, rays, and pith during dormancy, but disappears during the growing period (Swarbrick 1927, 1928; Wooldridge 1977). The unstratified vascular cambium over- winters as 5-10 layers of undifferentiated cells (Evert 1963b) (Fig. 6.6). Fusiform initials are 268-717 pm long, with overlapping ends and numerous depressed primary pit fields in the side walls.

Swarbrick (1927) reported that cambial activity began at the apex of a branch, proceeded basipetally, and ceased in October in England. Cambial cells swelled before dividing and produced xylem vessels.

270

Secondary phloem

CHARLOTTE PRATT

Fig. 6.6. Secondary vascular tissues of an apple stem in a 3-dimensional diagram showing transverse, radial, and tangential planes. Cambial zone has produced, on the right, secondary phloem, composed of sieve elements with sieve plates in lateral and end walls, companion cells, axial strands of parenchyma cells, some containing crystals, and ray parenchyma. On the left, cambial zone has produced diffuse-porous secondary xylem, containing vessels, fibers, fiber-tracheids, and ray parenchyma. The region of developing secondary xylem is greatly shortened. Contents and pits of all cells have been omitted. (Eames and MacDaniels 1947).

Swarbrick ignored phloem. These observations were not confirmed by Evert (1963b). Evert determined the period of cambial activity on the basis of mitotic figures alone. Fusiform initials slowly divided periclinally from early April to mid-May in Montana producing new phloem cells. The maximum rate of cell division occurred in June and early July. Mitoses ceased by the end of July or early August depending on the branch. Ray initials began to divide in mid-May at the time of new xylem formation, reached a peak in June, and ceased to divide in early July. The degree of activity varied with the branch.

Increase in trunk girth as an indicator of cambial activity in 2-year-old trees occurred from June to September, while total shoot growth increased from June to August, at Guelph, Ontario, Canada (Khatamian and Hilton 1977). In very old trees (40-70 years old) expansion occurred from May to August in Ithaca, New York (Knudson 1916).

Apple bark separated (“slipped”) through the cambial zone from early


April to mid-May, and through the youngest, thin-walled xylem from the end of May to the end of July or early August (Evert 1963b). Since grafting is done during the earlier period and budding in late summer, I conclude that both these techniques of vegetative propagation take advantage of the availability of dividing vascular cells.

There were no living sieve elements in the secondary phloem during dormancy (Evert 1963b). The first cells produced by cambial initials on the phloem side were 1-2 rows of precursors of fiber-sclereids and crystal-bearing parenchyma in most branches. The 4-6 rows of new sieve elements and companion cells present by May 2 1 in Montana equalled about */3 of the annual increment of secondary phloem. In the next 10 weeks, 2-3 more rows of new sieve elements and companion cells were produced. Secondary phloem was completed by the end of July or early August. Sieve elements ceased to function in conduction in late Septem- ber or October. Definitive callose developed on sieve areas. Sieve elements and empty companion cells collapsed by late November.

Precursors (fusiform initials or 2-3-celled parenchyma strands) of fiber-sclereids and crystal-containing parenchyma overwintered on the margin of the cambial zone, and differentiated in early June to early August (Evert 1963b). Fiber-sclereids showed intrusive growth. Their walls were initially nacreous, unevenly thickened, and lignified, with simple, or often ramiform, pits. The laterally expanding fiber-sclereids and crystal-bearing parenchyma crushed the remains of the sieve elements of year one, and then usually collapsed themselves.

Secondary phloem consists of sieve elements, companion cells, axial and ray parenchyma (Fig. 6.6) (Evert 1963a: MacDaniels 1918). A mature sieve element has lost its nucleus. It has a thin parietal layer of cytoplasm that contains plastids and carbohydrate granules and enters the pores of the sieve plates. The walls are nacreous at first, becoming thick. The end walls are transverse to very oblique (appearing wedge-shaped in tangential section and broad in radial section). Sieve plates are simple in transverse end walls, and compound in oblique end walls. The largest sieve plates are found in end walls. There are fewer sieve areas in tangential than in radial walls.

Most sieve elements have a companion cell: in cross-section it usually appears in a corner of the sieve element almost always next to a ray (Evert 1963a). At maturity its nucleus appears amorphous and may be nonfunctional. The wall between a companion cell and its sieve element is thin and pitted.

Axial parenchyma cells occurring in apple phloem were classified by Evert (1963a) according to their contents: (1) crystals, (2) tannin and/or starch, and (3) little or no tannin or starch. They originate from phloem initials. They occur in strands, each consisting of 2-31 crystal-bearing cells (Fig. 6.6), or 4-6 cells of each of the other two types. Growth rings in the phloem are delimited by (1) the fiber-sclereids and crystal-bearing

280 CHARLOTTE PRATT

parenchyma described above, if they are still present, and (2) late phloem parenchyma containing tannins and remaining turgid (Evert 1963b).

Secondary xylem was only briefly considered by Evert (196313). The first xylem cells to mature from cambial initials were vessels: maturation began in the third week of May in Montana. Secondary xylem ceased to differentiate in August at the same time as secondary phloem. Thus, the annual production of secondary xylem was accomplished in about 1 2 weeks while secondary phloem took 18 weeks.

Secondary xylem was more fully described by Eames and MacDaniels (1947). Apple wood is diffuse-porous and heavy because of numerous fibers and the thick walls of vessels, fiber-tracheids, and parenchyma [Fig. 6.6). Heartwood is darker than sapwood due to impregnating sub- stances, and is saturated with water. Vessels have bordered pits on the side walls and mostly simple perforations in the end walls (Eames and MacDaniels 1947; Solereder 1908). Xylem fibers and fiber-tracheids have bordered pit-pairs (Eames and MacDaniels 1947). Medullary rays travers- ing both secondary phloem and xylem are 1-3 (mostly 1-2) cells wide (Solereder 1908), and contain tannins and starch grains (Eames and MacDaniels 1947).

Schaffer and Wisniewski (1988) suggested that the ultrastructure of ray and axial xylem parenchyma cells adjacent to vessels and fibers may play a role in the freezing response of apple twigs 1-2 years old. After the secondary wall was formed in a parenchyma cell, endoplasmic reti- culum was conspicuous next to the pit membrane and along the adjacent wall, especially in the wall adjoining the vessel. The authors called this structure the “protective layer.” Later they preferred the term “anomalous layer” (personal communication), analogous to the “tylose or tylosis- forming layer” (Esau 1977). This is an extra, loose-textured wall layer between the plasma membrane and the secondary wall, or sandwiched between 2 secondary walls. It is thicker in the pit cavity.

Growth rings of even diffuse-porous wood are defined by differences in cell size, type, and arrangement between the late wood of year one and the early wood of year two [Eames and MacDaniels 1947). However, Doley (1974a,b) found no statistically significant differences between early wood and late wood in measurements of fiber width, wall thickness, vessel dimensions or distribution, or size of axial or ray parenchyma. All measurements were affected by the vigor of the composite tree and the width of the growth ring, which were influenced by the size-controlling rootstock and environmental factors.

Two growth rings in one year-a wide ring before harvest and a narrow ring after harvest-were formed in a bearing tree of ‘Red Astrachan’ (Tingley 1937). Such rings were called false annual rings by Eames and MacDaniels (1947).

When 1-year-old, container-grown apple trees were inverted during their second growth season, the branches curved toward their roots


(Mullins 1965). Reaction wood developed on the convex side of these branches. Usually called tension wood in dicotyledonous woody plants, reaction wood occurs on the upper side of branches (Esau 1965). It has fewer vessels and rays, and more fibers than normal wood. The walls of so-called gelatinous fibers in reaction wood have layers which contain cellulose, but no lignin. Both reaction wood and virus-induced “rubbery” wood have less lignin than normal wood, and the lignin differs in chemical composition (Scurfield and Bland 1963). A crotch is a major fork in the scaffold of an apple tree. The anatomy of

crotch angles was described by MacDaniels (1923). He stated that the secondary xylem in crotch angles differed from normal apple secondary xylem in having (1) more parenchyma, (2) larger and more irregular medullary rays, (3) fewer and smaller fibers and vessels, and (4) distorted vessels with simple rather than scalariform perforations. The cambium produced wider xylem rings within a wide-angle crotch than on the outer sides. Some xylem rings overlapped and strengthened the crotch. Cambium and bark became folded as the crotch filled with secondary xylem (Fig. 6.7 A). During this process the cambium shortened,

Fig. 6.7. Tree crotches in diagrammatic longitudinal sections. A. Burial of the base of a living branch by 10 growth rings [x’ to xlO). On the upper side of the branch, secondary xylem, cambium, secondary phloem, and cortex are folded as a result of confined growth in a narrow angle. Only the pith is unaffected. B. Weak crotch between approximately equal branches showing 5 growth rings and occluded bark. Cortex and phloem stippled; pith solid black. [Eames and MacDaniels 1947).

282 CHARLOTTE PRATT

apparently by loss of cells (Eames and MacDaniels 1947; MacDaniels 1923). In narrow-angle crotches cambium grew so slowly that bark was caught in the crotch angle (Fig. 6.7 B). Such a crotch is a site of winter- killing and splitting (MacDaniels 1923).

This interpretation of the structure of crotch angles has been elaborated. Eames and MacDaniels (1947) stated that masses of thick- walled xylem parenchyma may form in the crotch area, and that this is a source of weakness. The displacement of phloem and periderm from the crotch area results in concentric rings of raised bark around the base of a branch. Shigo (1985, 1986a,b) found at the branch-trunk junction “compacted xylem,” but he did not describe it histologically. He thought that it deterred the spread of micro-organisms between trunk and branch. In some crotches cracks separate the cambium and bark into parts which roll inward to form “occluded bark,” which occupies the space usually filled by compacted xylem. This type of crotch is subject to splitting. Branch cambium becomes active earlier in the spring than trunk cambium. The former produces at the base of a branch a ring of xylem which is overlaid by xylem from the trunk cambium later in the same season. Shigo called such growths “branch collars” and “trunk collars,” respectively. They form a strong and resilient ball-and-socket structure. This interpretation has not been investigated in apple.

Shigo (1986a) described and named codominant stems in pear, which were presumed to develop from 2 apical buds (Shigo 1986b). The bases of codominant stems were separated only by bark ridges: otherwise they were extensions of the trunk without collars or infection-resistant (“protective”) zones. I think that codominant stems imply either dichotomy of an apical meristem or the abortion of the shoot tip followed by development of the 2 uppermost axillary buds. Such bifurcations occur rarely in apple.

Bark includes not only periderm, but also the remains of the cortex, patches of primary phloem fibers, as many as 15-20 annual increments of nonfunctioning secondary phloem, and the cambial zone (Evert 1963a). According to Stebbins et al. (19721, bark contains rhomboidal and druse crystals in septate phloem fibers. This seems to be the only mention of septate phloem fibers in apple, and they may have been strands of crystal- bearing parenchyma cells. Internal phellogen may surround and isolate groups of primary phloem fibers (Evert 1963a). Toward the outside, it produces 6-10 layers of radially flattened cells of cork (phellem). These cells contain tannin, and have refractive tangential walls. Toward the inside, the phellogen produces 1-2 layers of phelloderm cells resembling cortical cells.

As the circumference of a branch or trunk increases, the smooth bark cracks, and some areas become depressed (Eames and MacDaniels 1947). The early periderm is being replaced by new, lenticular or shell-shaped, and overlapping patches of internal phellogen that originate at different


times in successively deeper tissues, such as cortex and secondary phloem. This is the beginning of scaly bark (rhytidome), which is well established in 6- to 6-year-old stems. The bark of large apple trunks has weakly defined, vertical ridges composed of periderm and dead phloem.

Lenticels in apple bark (Eames and MacDaniels 1947; Esau 1965) are composed of suberized cells with intercellular spaces (Esau 1977; Wutz 1955). As the stem thickens, lenticels break up into smaller lenticels separated by ordinary periderm (Esau 1965). Wherever new periderm is exposed, new lenticels develop from lenticel phellogens.

Rapid cambial growth causes wrinkles in the bark around the base of a branch (MacDaniels 1953) (compare crotch). Such wrinkles may persist even around the sites of dead branches because new phellogen adheres to, and adds to, old, wrinkled bark (Millington and Chaney 1973). This bark includes a complex of latent axillary buds and their traces, which lengthen to keep pace with wood and bark growth (MacDaniels 1953). They may develop into water sprouts years later.

The secondary anatomy of apple spurs has been investigated only in relation to their vegetative or flowering condition in biennially bearing cultivars. No consistent specification of spur length or thickness is reported. The cambium is more active in rate and duration of cell division in a nonfruiting spur, and so the growth ring is wider than in a fruiting spur (Christoff 1939; Crow and Eidt 1921; Finch 1935; Struck- meyer and Roberts 1942). Wide rings have few, scattered, thick-walled vessels, and narrow rings have many, large, thin-walled vessels (Christoff 1939; Finch 1935; Struckmeyer and Roberts 1942). A spur of an annually bearing cultivar resembles anatomically a nonbearing spur in a biennial cultivar (Christoff 1939). Data on relative amounts of parenchyma and fibers in xylem and phloem in fruiting and nonfruiting spurs are inconsistent, and do not take into account the larger bulk of vascular tissues in wide rings than in narrow rings. They are, therefore, omitted in this review. Anatomy of spurs may not be reinvestigated because modern cultivars and crop control measures encourage annual bearing.

V. LEAVES

A. Ontogeny A leaf primordium is initiated by periclinal divisions in T-2 or T-3 on a

flank of the apical meristem (Pratt et al. 1959; Rouffa and Gunckel 1951b). Procambium develops concomitantly in T-3 or T-4, proceeding acropetally around the gap of the leaf below from the procambium of the stem (Rouffa and Gunckel 1951b).

The leaf has 3 traces, each associated with a separate gap (trilacunar

284 CHARLOTTE PRATT

node) (Devadas and Beck 1971, 1972; Swingle 1927). The two lateral leaf traces divide in the leaf base; each outer branch supplies a stipule, and the inner branch enters the petiole with the median trace. In Rosaceae the procambial strands and, subsequently, primary phloem and primary xylem differentiate acropetally into the leaf (Devadas and Beck 1971) (See also Stems).

At the stage when a leaf primordium is a finger-like protuberance flattened on its adaxial side (MacDaniels and Cowart 1944), the stipules are represented by small primordia on either side of the base (Eames and MacDaniels 1947; Rouffa and Gunckel 1951b). The base of the leaf primordium is an intercalary meristem and forms the petiole, which develops concomitantly with the blade. The blade develops from 2 layers of cells derived from marginal and submarginal initials which produce a marginal meristem on the lateral flanks of the midrib. The superficial cells of the marginal meristems divide anticlinally to form epidermal cells, and small groups of subepidermal cells divide to form the rest of the blade. The subepidermal cells on the adaxial side will become the first row of palisade cells, and those on the abaxial side will form the spongy mesophyll. Cells between these 2 layers will form the central mesophyll and the smallervascular bundles. After 8-10 layers of cells are formed, or when the young leaf is 4-15 mm wide, blade thickness is essentially established. Periclinal divisions cease except in the veins and some other areas. The blade expands in length and width by anticlinal divisions and cell enlargement.

The ontogeny of the apple leaf was interpreted differently by 2 stu- dents of periclinal cytochimeras of apple. Dermen (1951) found that the ploidy of veins was always the same as that of the surrounding mesophyll in a 2x-2x-4x chimera. His observations confirmed MacDaniels and Cowart’s (1944) description of leaf development. Blaser and Einset (1948), however, found that the major vascular system developed independently of, but concomitantly with, the mesophyll. The midrib and primary veins developed from the leaf traces, and smaller veins developed in the marginal meristems. The former might have a ploidy different from that of the mesophyll, and the latter the same ploidy as the surrounding mesophyll. These conclusions, drawn from developmental studies of 2x-4x- 4x, Z X - ~ X - ~ X , and 2x-2x-2x-4x chimeras, did not support MacDaniels and Cowart’s (1944) contention that all tissues of the blade developed from 2- layered marginal meristems.

Before air spaces (lacunae) appear, epidermal and subepidermal cells elongate perpendicularly to the leaf surfce (MacDaniels and Cowart 1944). On the adaxial side subepidermal and central meristematic cells differentiate into 1-3 more layers of palisade cells, depending on the size and position of the leaf, environmental factors, and even the rootstock (Beakbane 1967b).

Mitoses cease first in the parenchymatous sheaths of large veins


Fig. 6.8. mesophyll, minor veins, stomates, and a hair. (MacDaniels and Cowart 1944).

Apple leaf in 3-dimensional diagram showing epidermis, palisade cells, spongy

(MacDaniels and Cowart 1944). Palisade cells divide anticlinally after the upper epidermal cells have stopped dividing. Cell divisions in the spongy mesophyll cease before those in the abaxial epidermis. During the expansion of the leaf, spongy mesophyll cells separate into filaments attached to epidermal cells, except guard cells, at one end and to palisade cells and veins at the other end. Chloroplasts develop in the parenchyma of the midrib before they develop in the mesophyll.

B. Maturity The mature apple leaf has been described and illustrated by Beakbane

(1967b), Krapf (19671, and MacDaniels and Cowart (1944) (Fig. 6.8). The adaxial cuticle consists of a layer of wax and cutin containing electron- opaque, anastomosing microfibrils, and electron-translucent lamellae (Hoch 1975,1979). The inner part of the cuticle contains polysaccharides (Reed and Tukey 1982). The adaxial epidermal cells are irregularly rectan- gular in surface view, except over the veins, where the cells are elongated parallel to the long axis of the vein (MacDaniels and Cowart 1944).

The abaxial epidermal cells have thinner cuticle than the adaxial

286 CHARLOTTE PRATT

epidermal cells. They are variable in thickness and shape, except for the paired, kidney-shaped guard cells, which are nearly constant in size within a cultivar (MacDaniels and Cowart 1944). The cellulose walls of guard cells are thinner adjacent to epidermal cells, and thicker adjacent to the pore and on the inner and outer sides. Increase in turgor causes the thin walls to stretch, and the ellipical pore opens. Guard cells have denser protoplasm, a less conspicuous vacuole, and a larger nucleus than do other epidermal cells. Guard cells contain green plastids smaller than the chloroplasts of mesophyll cells. There are no stomates over small veins, and only a few over the midrib and larger veins. The density of stomates varies with the vigor of the shoot, leaf size and position, and environmental factors. Stomates of widely varying overall size, shape, and pore size were present in apple leaves collected in April in England (Slack 1974). Stomates were functional (defined as elliptical with clearly defined pores) in June. Distribution of stomates over the leaf surface was variable, although ‘Cox’s Orange Pippin’ leaves had significantly more stomates per unit area than those of ‘Golden Delicious’.

Apple epidermis has the following structures (Lewis 1968; Metcalfe and Chalk 1950): (1) Unicellular hairs originate from single epidermal cells (Fig. 6.8). They are abundant on both surfaces of young leaves, but in mature leaves they occur mostly on the abaxial surface. (2) Simple hydathodes, associated with vascular tissue, occur on the adaxial surface at the margins and tips of leaves, and at the ends of very minorveinlets. (3) Glandular hairs or trichomes, also called “extrafloral nectaries” (Metcalfe and Chalk 1950) or “colleters” (Blaser and Einset 1948), occur abundantly along the adaxial sides of main veins and at the tips of serra- tions. They develop from epidermal and subepidermal cells adjacent to developing vascular bundles in young leaves (Blaser and Einset 1948; Lewis 1968; MacDaniels and Cowart 1944). Glandular hairs have a multicellular, parenchymatous stalk, and a multicellular head containing reddish-brown pigment. The head has an epithelial layer of radially elongated cells with dense protoplasts and conspicuous nuclei. These cells are covered by cuticle except for the two terminal ones termed “nectarodes” by Lewis (1968) and thought to release the secretions. The central column of the head consists of vertically elongated secretory cells with conspicuous nuclei. Lewis suggested that the secretions favored the growth of parasitic organisms, such as fire blight bacteria.

Each mature palisade cell is surrounded by air space continuous with that in the spongy mesophyll, except in the vicinity of a vein. There may be 3-4 layers of palisade cells in leaves on vigorous shoots, but only one layer in some shaded leaves or in small, basal leaves.

The supporting and conducting system of the leaf blade is continuous with the vascular system of the stem through the petiole bundles (MacDaniels and Cowart 1944). Distal to the departure of the stipule traces from the lateral traces, the 3 leaf traces in the petiole join into a


single, crescent-shaped, collateral vascular bundle surrounded by cortex containing localized chlorenchyma, and epidermis with a few stomates. Primary xylem on the adaxial side of the bundle grades into secondary xylem. Primary phloem, on the abaxial side, has small, thin-walled, irregular sieve elements and fibers. Druses occur in phloem parenchyma cells, and rhomboidal crystals in phloem septate fibers; few druses occur in xylem parenchyma cells (Stebbins et al. 1972). This appears to be the only mention of septate phloem fibers in apple petioles; the so-called “fibers” may have been strands of crystal-bearing parenchyma cells. Cambium is well developed, producing secondary xylem and phloem (MacDaniels and Cowart 1944; Stoutemyer 1937).

The midrib runs from the base to the apex of the leaf (Krapf 1967; MacDaniels and Cowart 1944). Structure of the midrib is similar to that of the petiole; its abaxial sheath includes collenchyma and sclerenchyma (MacDaniels and Cowart 1944). From the midrib primary veins extend to the margins of the leaf. They branch into secondary and tertiary veins, which end in small, definite islets of mesophyll (Eames and MacDaniels 1947). The vein ending consists of one spiral or reticulate tracheary element and one parenchyma cell (transition cell) representing a phloem mother cell which did not divide. All the veins, even the endings, are surrounded by a parenchymatous bundle sheath (Fig. 6.8). The bundle sheaths of large veins meet the epidermis on both surfaces. Rhomboidal crystals may be present in sheath cells.

Apple leaves vary in thickness depending on the degree of exposure to light in various positions in a canopy; thickness is related to specific leaf weight and the number of palisade layers (Cowart 1935; Doud and Ferree 1980; Jackson and Beakbane 1970; Wooge and Barden 1987). Leaves of long shoots and bourse shoots are thicker and larger than those of fruiting spurs (Cowart 1935; Struckmeyer and Roberts 1942). The thinnest leaves occur on shaded, nonfruiting spurs. The spongy mesophyll has a greater proportion of air spaces under low light than it does under high light (Jackson and Beakbane 1970).

The formerly used pesticides, lime-sulfur and arsenate of lead, reduced photosynthesis and increased the ratio of internally exposed surface to externally exposed surface (Pickett and Birkeland 1941,1942). Palisade cells in the adaxial row were fewer, deeper, and wider in sprayed than in unsprayed leaves.

The abscission zone at the base of the petiole seems to consist of small cells (Simons 1977). The details of leaf abscission and periderm formation of the leaf scar were not specified for Malus (Eames and MacDaniels 1947).

C. Growth Rates Growth rates of apple leaves and internodes were studied in stoolbed

shoots of Crab C rootstock in England. The length and width of the leaf

200 CHARLOTTE PRATT

and the length of the internode reached 50% of their final dimensions at about the same time (Hancock and Barlow 1960) depending on the rate of shoot growth (Barlow 1980). The growth of leaves 10 mm long to full length followed a sigmoid curve (Barlow and Hancock 1958). Total mitotic activity was maximal when the leaf was about 15% of its mature size (Barlow 1974), but a high rate of division in palisade cells continued until the leaf was 70% of its final size. Rapid cell division in other layers of the leaf continued until the leaf was 30% of its final size, or 5 days after the maximum rate of division of all tissues. The maximum rate of increase in area occurred at the same time. Except in the palisade cells, increase in leaf volume occurred throughout the period of leaf growth. Leaf growth rates were influenced by environmental factors (Hancock and Barlow 1958).

VI. VEGETATIVE PROPAGATION

A. Adventitious Roots

Adventitious roots emerge from the axil of a bud, beside or below a bud, or from an internode (Gardner 1937). Ease of rooting and origin of roots vary with the cultivar. Doud and Carlson (1977) reported that roots were initiated in bud and leaf gaps where starch content was high. Etiola- tion of the base of the cutting increased starch content, decreased amount of primary phloem fibers, and increased rooting in their experiments.

Clonal rootstocks are usually propagated from mother plants or stools, whose bases are covered with soil to stimulate rooting. The role of light in adventitious root formation is not well understood. Low light has been reported to retard the formation of primary phloem fibers, which may inhibit rooting (Beakbane 1961,1969). However, Christensen et al. (1980) reported that low light intensity increased the amount of primary phloem fibers in apple stems.

Upshall (1931) ascribed ease of rooting to the absence or paucity of pericyclic (phloem) fibers in French Crab seedling roots compared to the abundant fibers in the roots of hard-to-root cultivars. The vessels of detached root cuttings of many cultivars and old seedling trees contained gum within a week of planting, but gum did not inhibit rooting.

Wounding the base of apple cuttings to increase callusing and rooting is thought to produce gaps in the sheath of primary phloem fibers. Pontikis et al. (1979) noted that primary phloem fibers are interrupted by the emer- gence of leaf and bud traces at a node. Nodes are more frequent at the base of a stem, and so more gaps occur there than at more distal locations. Two vertical incisions were made through the bark of an internode of a woody cutting, which was then treated with indolebutyric acid and bottom heat. Callus developing from the adjacent, uninjured cambium filled the inci-


sion, and some adventitious roots developed from this callus. Howard et al. (1984) and MacKenzie et al. (1986) stimulated rooting by splitting the base of a hardwood cutting before treatment with indolebutyric acid. In the split halves of the stem, callus developing from cortex, phloem, and cambium formed nodules separated by slower-growing ray tissues. Within these nodules new cambium and randomly oriented, lignified xylem cells differentiated in the callus. Root primordia arising near new cambium eventually linked up with the vascular cylinder of the cutting. Unfortunately, the initiation of root primordia was not investigated.

These accounts are based on the assumption that apple stems have no pre-formed root primordia or “germs” (Eames and MacDaniels 1947). However, Swingle (1927) found them in some apple cultivars; they were present in the primary body at branch gaps, leaf gaps, and primary and secondary medullary rays. The traces of such root primordia may elongate and even branch for 2-3 years before emerging either as burr knots or as adventitious roots. Burr knots are not caused by the crown gall organism, Agrobacterium tumefaciens (Smith and Townsend) Conn (Swingle 1925), but are a genetic character in some families of seedlings (Cummins and Aldwinckle 1983). Burr knots may provide an entrance for fire blight bacteria or harmful insects, and if very large, may inhibit or deform the growth of the seedling.

B. Adventitious Shoots

1. On Roots. The induction of adventitious shoots on detached pieces of apple root (root cuttings) is a method of vegetative propagation which provides own-rooted trees. Such shoots were thought by Stoutemyer (1937) to be juvenile. Although they tend to flower sooner than seedlings, they do not root readily, and so Robinson and Schwabe (1977) did not con- sider them juvenile. Induction of shoots from adventitious roots is a method of determining the phenotype of L-I1 and L-I11 of periclinal chimeras (Decourtye 1987; Decourtye and Lemoine 1988; Lacey et al. 1978).

Adventitious buds originate from root tissues from the pericycle to the periderm (Robinson 1975). They develop from groups of meristematic cells in otherwise undifferentiated parenchyma. The apical meristem and one or more leaf primordia are formed before a procambial connection develops basipetally, acropetally, or both, to the cambium. Robinson, as well as Robinson and Schwabe (19771, Kanazawa et al. (1978), and others, concluded that the inconsistent reports of the initiation of shoots may reflect the difficulty of finding the earliest stages of ontogeny.

Older roots may form adventitious buds late in the growing season in the cortex opposite a secondary phloem ray (Siegler and Bowman 1939). This suggests that, in detached roots at least, the entire cortex is not shed

290 CHARLOTTE PRATT

when the vascular cambium becomes active. Another explanation may be that in older roots buds originate from the pericycle, which was called “secondary cortex” by Stoutemyer (19371, or “lenticel meristems” of the periderm by Lacey et al. (1978).

Suckers grow from the roots of trees when the scion becomes weak or dies. Their origin seems not to have been investigated. We may assume that they originate endogenously as in root cuttings (Esau 1965).

2. On Stems. The induction of de novo shoots on stems with secondary vascular tissue has been proposed as a method of obtaining “juvenile” (easily rooting) shoots of cultivars, or of obtaining shoots expressing the inner phenotype of a periclinal chimera. These shoots differ from those from latent or dormant buds, which are axillary buds, particularly on spurs, which may be buried in old apple stems (MacDaniels 1953; Stoutemyer 1937). The traces of latent buds elongate, but retain their origin in the primary tissues of the vascular cylinder. When latent buds emerge on limbs of old trees they are called water sprouts; cuttings from them do not develop adventitious roots.

Adventitious shoots arise from centers of meristematic activity, called “sphaeroblasts” (Baldini and Mosse 1956) or “sphaeroplasts” (Stoutemyer 1937). They arise in the cortex and outer phloem of 2-year-old stems from which all axillary buds have been removed. Sphaeroblasts may become lignified or they may develop into shoots, which become connected by callus cells to the phloem, usually a phloem ray, and to the xylem. As the bud grows outward, its procambium becomes continuous with the cambium of the stem. Stoutemyer (1937) considered these shoots to be juvenile, but they do not root readily.

When Dermen (1948, 1955, 1958) disbudded young trees of periclinal chimeras of apple, shoots developed from the outer phloem and emerged at the internode. He called such shoots at first adventitious (Dermen 19481, but later he called them endogenous (Dermen 1955, 1958). They arose from sphaeroblasts (which he did not describe), and have a trace not continuous with the pith. He concluded on the basis of ploidy that such shoots arose from L-I1 or L-111.

C. Grafting

1. Wound Repair. The anatomy of wound repair is important in pruning and otherwise maintaining the tree, and relates to budding and grafting. A common type of injury occurs during the pruning of branches. At the cut surface, vessels, tracheids and other cells are soon plugged by wound gum composed of lignin and tannins (Swarbrick 1926a). The division of living cells (cambium, axial and ray parenchyma of the secondary xylem) produces abundant callus within which a new cambium forms and pro-


duces new fibers, tracheids, and chains of short vessels [wound wood) (Bradford and Sitton 1929; Krahmer 1981). This callus is thick and advances like a wave from the periphery towards the center of the cut surface. Phellogen develops in the callus, but the resulting bark on top of the callus wave advances more slowly than the rest of the wave. This process is called “overwalling.” If a branch is pruned to induce a lateral branch to become a leader, the growth of surface callus and consequent overwalling is greater on the side toward the new leader. New xylem elements become oriented in the direction of the new leader. Surface wounds made by the removal of bark heal in a similar sequence of wound gum, surface callus, and overwalling.

Girdling or ringing is the removal of bark to stimulate flowering or to increase fruit retention. Swarbrick (1926b) found that prevention of drying by covering the ringed area with adhesive tape increased the amount of callus. If ringing was done before June 16 in England, callus developed from the cambium on the distal edge of the ring. If ringing was done after June 16, callus developed from both edges. If the wound was not covered, no callus developed from the proximal edge. Soe (1959) confirmed these observations, and noted, as did MacDaniels and Curtis [1930), that new phellogen developed in callus before new vascular cambium appeared and formed wound wood.

When a spiral ring was made, MacDaniels and Curtis (1930) found that the first vessels had porous openings in the radial walls; later vessels had open ends and were oriented along the axis of the spiral. Soe (1959) also observed orientation of vessels in the direction of the spiral.

2. Budding. Budding is the insertion of a bud attached to a slice [shield) of bark and wood under the bark of a rooted rootstock tree 1-2 years old. This is normally done when vegetative growth is slowing down in late summer, but the bark still slips. Union of stem tissues begins at once. The stock is decapitated before the inserted bud begins to grow the following spring [Brase 1956: Way et al. 1967).

Budding is used extensively to propagate, and experimentally to test transmission of virus diseases. Three types of budding are shield-T-, shield-inverted T-, and chip-budding.

In T-budding, [Fig. 6.9) a T-shaped cut is made in the bark of the internode of a stock tree. When the bark flaps are lifted, the bark separates through the youngest xylem, which still has unlignified vessels. A bud shield is inserted between the flaps and tied securely with a rubber band. The function of the flaps is to hold the shield in close contact with the young xylem of the stock: the flaps do not become part of the composite tree.

The injured cells of the shield and stock die and form a necrotic plate [Bailey 1923; Mosse 1962; Mosse and Labern 1960; Wagner 1969). The plate is composed of broken cell walls and other cell debris [Wagner

292

Bud /-l

CHARLOTTE PRATT

.Callus ~ P h l a c m =Cortex

--- Cambium Callus t i ssue

mi Xylem Primary phloem f i b r e s

Fig. 6.9. Apple T-bud union in diagrammatic transverse sections. A. Callus being produced from the parenchyma of the secondary xylem of the stock: 3 weeks after budding. B. Space between the bud shield and the stock is filled with callus in which a new cambium connects with the old cambium of the bark flap and the bud shield: 8 weeks after budding. (Mosse and Labern 1960).

1969). Axial and ray xylem parenchyma of the stock, cambium cells of the bark flaps, as well as living cells of the cortex and cambium of the shield, divide within a day or two to form callus. The stock contributes more callus than does the shield. Within a week, callus has broken through the necrotic plate forming callus bridges between scion and stock (Bailey 1923; Bradford and Sitton 1929; Mosse 1962; Mosse and Labern 1960; Wagner 1969). Scattered tracheids differentiate in the callus (Mosse 1962). New cambium differentiates in the callus, and becomes continuous with the old cambium in the bark flaps and in the shield within 3- 4 weeks of budding (Fig. 6.9) (Bailey 1923; Mosse 1962; Mosse and Labern 1960). As the cambium shortens, callus becomes lignified, and the bud shield is held in a firm union. Eventually the cambium comprises only the cambium of the bud shield and the stock, and produces phloem and xylem as in healed wounds.

Mosse and Labern (1960) reported nodules of two types in callus of young bud unions. The nodules were spherical, composed of a vascular center and a cambial sheath. Amphicribral [phloem peripheral and xylem


central) nodules developed in callus derived from phloem parenchyma in bark flaps, and, less commonly, in the bud shield. Amphivasal [xylem peripheral and phloem central) nodules were more frequent than amphicribral nodules, and occurred in callus derived from xylem parenchyma. They seldom contributed to new cambium, except for some large, coalesced, amphivasal nodules. They were similar to the nodules in ring-grafted stems [Mosse 1953) or grafts between components varying in diameter [Sass 1932). The cause of nodule formation is unknown, but the authors did not regard them as indicators of incompatibility.

Shield-inverted T-budding differs from T-budding in that an inverted- T-cut is made in the stock [Howard et al. 1974; Skene et al. 1983). The authors thought that the former method was superior to T-budding because there was closer contact between the shield and the stock below the bud, and less callus was needed to fill the space at the end of the first growing season. In the second season, 2045% of the nursery trees, depending on which of the five clonal stocks were used, were large and well branched [Skene et al. 1983).

In chip-budding, a dormant bud attached to a wedge of bark and xylem is inserted into a similarly shaped notch in the stock and tied. The cambia of both components must be aligned. At the end of the first season, little callus was found, and both cambia had produced new xylem. In the following season, 5488% of the budded nursery trees, depending on the clonal rootstock used, were large and well branched [Skene et al. 1983). The authors concluded that chip-budding produced the best results in healing of the bud shield, and in production of good nursery trees.

3. Other Grafting Techniques. The scion may be a dormant stem piece, usually one year old, with one or more buds [Hartmann and Kester 1983). The scion is inserted [grafted) into a rootstock, which may be a dormant, rooted seedling or cutting, a layered plant, such as a clonal rootstock from a mother plant in a stoolbed, a detached root, or a nursery or orchard tree [Brase 1956; Way et al. 1967).

Whip-and-tongue or whip grafting is usually done indoors during the winter with dormant nursery stock, and thus is also called “bench grafting.” The base of the scion and the top of the rootstock are first cut diagonally, and then a slanting cut is made in each. The tongue of each is inserted into the cut of the other. The cambia of scion and stock must be in firm contact with each other.

A tongue, wedge, or cleft graft may be done indoors on dormant nursery stock in winter, or in the orchard on dormant trees in early spring. The latter is also called “top-working.” The stem of the stock is cut transversely and split. The base of the slender scion is cut to a wedge shape and inserted into the cleft on one or both sides of the stock. The cambia of both components are aligned and held under pressure exerted by the cleft.

In a tongue graft [Sass 1932) callus is produced from the cortex,

CHARLOTTE PRATT 294

cambium, and secondary phloem of both components, but not from periderm, secondary xylem, or pith. When the new cambia form a continuous sheath, new secondary phloem and xylem, which are essential for a strong union, are produced. New phellogen differentiates from surface callus cells, and forms new periderm. The remaining callus becomes sclerified centripetally. The central spaces of the graft may or may not become filled with callus.

When the components of a graft are of different diameters, the excess callus “lips” may contain knots, or whorls of meristematic cells around centers of contorted xylem cells (Sass 1932). Knots are usually found in the scion and may persist for the life of the tree (see also Budding).

In order to demonstrate whether callus cells from scion and stock mix in the early stages of healing, pieces of bark from an apple cultivar with red (purple) xylem were grafted on the stem of a cultivar with white (colorless) xylem (Roberts 1934, 1937; Sax and Dickson 1956; Yeager 1944). In all cases the new xylem was colored, leading to the conclusion that the callus cells from the graft components had not mixed. However, Tubbs (1973) and Hartmann and Kester (1983) feel that callus and cambial cells mix or interlock in a successful union.

Sax and Dickson (1956) also experimented with the influence of polarity on healing of bark grafts differing in wood color from the stock. If the bark grafts were inverted or transversely oriented, the rate of healing was slower than in vertically oriented bark grafts, but the new xylem was always vertically oriented, and the same color as that of the source tree. Growth of the tree was inhibited until normal polarity resumed.

Ring-grafting has been done experimentally to induce dwarfing (Roberts 19341, as can be done also with an intermediate stem piece (Brase 1956; Way et al. 1967). Mosse (1953) made ring grafts from 2 dwarfing, clonal rootstocks (3426 and M.9) on a very vigorous rootstock (M.16), which was later budded above the ring with a cultivar. The trees were examined 3 years after budding. The bark rings had split and were bridged by tissues developing from coalesced, concentric bundles of M.16 under the M.9 ring. The narrow bark, color of wood, proportion of fibers and parenchyma, but not of vessels and fibers, were all characteristic of M.16, not of the dwarfing stocks. The trees were not small. Mosse (1953) concluded that the dwarfing effect was lost when the bridges of vigorous stock were formed, and that the scion, ‘Cox’s Orange Pippin’, reduced the vessel area and increased the ray area of M.16. Little or no effect of scion on vigor and yield was reported by Beakbane (1941) and Beakbane and Rogers (1956).

4. Incompatibility. Where the bud fails to unite with the stock (incompatible union), cambium is unorganized at the point of union, and the space is filled with callus which does not lignify [Jawanda 1968; Mosse


1962). Bark from the stock grows inward, and widens the gap between bud and stock. No fibers, vessels, or sieve elements occur at the union, and phloem begins to degenerate.

Other grafts may heal at first, but fail to maintain cambium continuity at the end of the first growing season (Bradford and Sitton 1929). Such a union and its components are said to be incompatible (uncongenial in Bradford and Sitton’s terminology]. Another symptom of incompatibility is the breakdown of newly formed vascular tissues. Mistakes in the alignment of cambia may cause swelling of the union, but this in itself is not due to incompatibility. Reliable indicators of incompatibility in grafting (Argles 1937) are excessive callus at the union without differentiation into cambial or vascular tissues, and clean horizontal breakage of the tree at the union, especially years after grafting, or when the tree begins to fruit.

Three types of incompatibility (Simons 1987) are: (1) nontranslocated, which is overcome by an intermediate stem piece between scion and rootstock: (2) translocated, which is not so prevented: and (3) that which is “induced between two normally compatible components by top working with another [incompatible?] variety.” Other symptoms of incompatibility observed by Simons in many studies of graft union failure were summarized in 1987. Failure of unions was traced back to abnormal cambial activity producing vascular tissues with disturbed orientation, to irregular distribution of vascular elements, or to early senescence. These abnormalities may be related to genetical differences between the cambia.

Robitaille and Carlson (1970) sought a method of using anatomical characteristics to predict compatibility of graft components. Five apple species were whip-and-tongue grafted onto 6 clonal rootstocks. At the end of the first growing season, the nursery trees ranged from no graft take to complete union, and sample unions were examined histologically. Only 2 out of 20 anatomical differences between scion and stock were significantly related to graft take: vessel density and diameter of tracheary elements. The authors, like Lockard and Schneider (19811, speculated that graft compatibility, at least during the first year, may depend on the structural similarity of the two component xylems.

VII. SIZE-CONTROLLING ROOTSTOCKS

Certain clonal apple rootstocks limit the size of the composite tree and promote precocious flowering. The mechanism of this interaction is still unknown. Rootstock breeders, especially in England, have tried to find morphological and anatomical differences in clones which might be useful in selecting seedlings.

Beakbane and Renwick (1936) reported that if the bud union were

296 CHARLOTTE PRATT

below ground level a cultivar grafted on the dwarfing stock M.9 tended to produce adventitious roots from the scion and to grow into a full-sized tree. The adventitious roots of M.9 were characterized by much smaller secondary xylem vessels, more secondary xylem parenchyma, and fewer secondary phloem fibers than the roots from the cultivar scion. The bark (all extra-cambial tissues) was thicker relative to the total transverse area in roots of M.9 than in roots of more vigorous stocks (Beakbane and Thompson 1939).

These observations suggested that root structure might be used to predict the degree of dwarfing by seedling rootstocks (Beakbane and Thompson 1939; Beakbane et al. 1941). A wide range of bark and wood characteristics were investigated in many Malling stocks varying in size control (Beakbane and Rogers 1956; Beakbane and Thompson 1947; McKenzie 1961a). The ratio of living tissue (axial and ray parenchyma) to dead tissue (vessels and fibers) in secondary xylem correlated well with the bark/wood ratio in rootstocks representing extremes of vigor, but less well in rootstocks in the middle range.

Bark/wood ratios calculated from transverse sections varied with age and, especially, fruiting of the composite tree (Mosse 1952). Mosse also noted that a very vigorous rootstock induced many more secondary phloem fibers in the narrow bark of the scion, while a dwarfing stock induced thicker bark with fewer phloem fibers. Fruiting tended to limit vegetative growth, especially in trees on dwarfing stocks. The anatomical similarities in dwarfing apple rootstocks, low vigor trees, and trees treated with a growth retardant, daminozide, have been pointed out by Jaumien and Faust (1984).

In Italy, Tomaselli and Refatti (1961) used the criteria of Beakbane and Thompson (1947) to compare 9 seedlings of open-pollinated ‘Starking Delicious’. As rootstocks, the seedlings induced low to excellent vigor 2- 6 years after grafting. Correlations of vigor ratings between years, and between vigor and bark thickness and fiber content, and proportions of living and dead tissues in xylem were poor and inconsistent. They concluded that such relationships cannot be used to select potential rootstocks. The validity of this conclusion may be questioned because of the small population and limited genotypes used.

Certain leaf characteristics have been proposed as additional indicators for early selection of size-controlling rootstocks (Tubbs 1973). Leaves of ungrafted dwarfing rootstocks have fewer palisade cells per unit area of leaf surface, but wider palisade cells with more intercellular air spaces, and fewer layers of palisade cells than those of vigorous rootstocks (Beakbane 1967b). Scions of low or intermediate vigor tend to be more influenced by an invigorating rootstock than more vigorous scions. The density of stomates increases with increasing vigor of a series of size- controlling rootstocks (Beakbane and Majumder 1975; Pathak et al. 1976).


A spontaneous 2x-4x-4x sport of the vigorous M.13, when used as a rootstock, produced very dwarf, precociously fruiting trees, too small for practical use (Beakbane 1967a). This rootstock had wide bark, narrow vessels, and wide rays like other dwarfing stocks, but a high percentage of secondary phloem fibers like M.13. This appears to be the only attempt to use a tetraploid sport, which is typically slow-growing, as a rootstock.

Tubbs (1973) summarized the literature on the structural characteristics of roots, stems, and leaves of rootstocks associated with low or high growth potential. He suggested that the physiological and anatomical interactions between stem and root cambia, and secondary growth in a composite tree should be considered rather than the effects of single factors on vigor.

VIII. COMPACT OR SPUR MUTANTS

Compact or spur mutants have arisen spontaneously in several widely planted, commercially important cultivars [Arasu 1968; Ferree 1988). They are generally distinguished from the standard strain by shorter extension shoots, due to shorter internodes, more fruiting nodes per branch, and greater leaf area per spur. Compact trees resemble trees on dwarfing rootstocks in having short internodes, but the latter do not exhibit thicker internodes and thicker leaves (Arasu 1968). Increased yield from spur sports was attributed to longer fruiting life of spurs in compact mutants than in standard strains (Walsh 1981).

Leaves of compact mutants are thicker, due to more palisade cell layers, than leaves of standard cultivars (Arasu 1968; Grossi 1976; Lapins and Fisher 1974; Liu and Eaton 1970; Westwood and Zielinski 1966). These thicker leaves resemble those produced by growth retardants, with minor differences in proportions of palisade cells (Arasu 1968; Eaton and Liu 1970; Liu and Eaton 1970).

Morphological features of spur sports may vary with the cultivar. In nonbearing trees, Walsh and Miller (1984) found that increased bud break of spurs on second-year branches was characteristic of all the compact mutants studied; short internodes on current season’s shoots occurred in ‘Delicious’ and ‘McIntosh’ spur sports, but not definitely in ‘Rome’ and ‘Granny Smith’ spur mutants. The authors speculated that the interaction of flower bud precocity and growth habit would complicate the distinction of spur and nonspur clones in bearing trees.

Frequency of reversion to standard habit differs in spur strains (Ferree 1988). Reversions suggest the possibility of a periclinal chimera (Pratt 1983; Pratt et al. 1967). The structure of two possibly chimera1 sports is hypothesized as follows. The somatic origin of a mutation is best demonstrated when it is found as a limb sport, as was the spur mutant ‘McIntosh

CHARLOTTE PRATT 298

Wijcik’ (Looney and Lane 1984). This mutant is not known to revert to standard habit. It transmits spurriness to 40-509‘0 of its progeny (progeny test) (Lapins 1969). Lapins (1974) therefore hypothesized that the gene mutation, called Co, was in L-11, whereas unstable spur mutants of ‘McIntosh,’ which did not transmit the gene, had the mutation in L-111. Decourtye and Lemoine (1988), by means of the progeny test and the adventitious root test (see Adventitious shoots, On Roots) demonstrated that ‘Stark Golden Spur’, an unstable spur sport of ‘Golden Delicious’, has the mutation in L-11. One adventitious shoot from a root of the original sport had the spur habit, and was hypothesized to have Co in L-I1 and L- 111, and to be stable.

IX. CONCLUDING REMARKS

The purpose of these reviews of apple morphology and anatomy (Pratt 1988, and the present paper) is to organize and communicate previously published information. Old apple literature tends to become buried, and hence unavailable to younger generations of research workers. The current research emphasis is on apple tree physiology, leaving little time for morphological and anatomical investigations. My reviews attempt to provide this background in a convenient format, with the hope that they will also stimulate new research in these areas.

Apple tree structure is generally similar to that of other dicotyledonous, woody plants. A feature peculiar to apple and closely related rosaceous plants is the phi layer in the cortex of roots.

Some unresolved structural problems are: (1) The organization of the secondary xylem in branch-axis junctions should be reworked in the light of Shigo’s ball-and-socket analogy. (2) Is the tendency of apple tree crotches to split due to a large proportion of parenchyma in the wood, to occluded bark, or to Shigo’s “compacted xylem”? What is the ontogeny and histology of the latter? (3) Do Shigo’s “codominant stems” in pear occur also in apple? How do they originate? (4) Are the phyllotaxy and secondary vascular structure of spurs related to their flowering? (5) What is the ontogeny of the mesophyll and veins of apple leaves? (6) The possibility of periclinal chimeras in apple somatic mutants (sports) should continue to be investigated by means of the progeny and adventitious shoot tests.

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