review. the control of flowering in wheat and - annals of botany

Annals of Botany 82 : 541–554, 1998Article No. bo980733

REVIEW

The Control of Flowering in Wheat and Barley: What Recent Advances in

Molecular Genetics Can Reveal

R. K. M. HAY*†‡ and R. P. ELLIS§

*Department of Plant Science, McGill Uni�ersity, Montreal, Canada, †Scottish Agricultural Science Agency, East

Craigs, Edinburgh EH12 8NJ, UK and §Scottish Crop Research Institute, In�ergowrie, Dundee DD2 5DA, UK

Received: 22 May 1998 Returned for revision: 30 June 1998 Accepted: 29 July 1998

The combined forces of developmental biologists, studying primordium initiation at the stem apex, and mathematicalmodellers, developing simulations of crop growth and development, have brought about considerable advances in theunderstanding of the control of flowering in wheat and barley. Nevertheless, there are still major gaps in thisunderstanding including: what determines the basic rate of development (magnitude of the phyllochron orplastochron) ; how temperature and photoperiod interact to bring about the transition from vegetative toreproductive development ; and how flowering occurs eventually in the absence of inductive conditions. Althoughgeneticists have tended to measure cereal flowering in terms of ‘days from sowing or emergence to heading’, resultsof studies using aneuploids and molecular markers are compatible with the roles for photoperiod and low-temperature vernalization established in purely-physiological or developmental investigations. They have alsorevealed the existence of ‘earliness per se ’ loci, whose detailed roles have yet to be established. Progress towardsisolating and characterizing wheat and barley loci is hampered by the poor resolution of mapping (location to aprecision of tens of thousands of base pairs). Neither of these broad approaches promises a rapid resolution of thefactors controlling the induction of flowering. Two expanding areas of molecular genetics now provide potential forgreater understanding of cereal flowering. First, the extensive homoeology among members of the Gramineae can beemployed to establish the existence and location of genes or quantitative trait loci in rice which correspond tocontrolling loci in wheat or barley. Since the rice genome is 1}30th of the size of the wheat genome, the accuracy ofmapping loci can be much higher, and there is greater potential for precise location of loci using techniques such aschromosome walking. With the ultimate cloning of individual genes, and the isolation of gene products, the relativeroles of the 20 loci apparently involved in the induction of flowering of wheat could be explored. However, progressin the molecular genetics of Arabidopsis (the second area) may provide a more rapid route to understanding thecontrol of flowering in cereals for several reasons : its small genome (1}4 that of rice) ; the likelihood of extensivehomoeology with cereals, in spite of differences in codon usage between monocots and dicots ; the existence of a widerange of flowering-time mutants ; and the control of floral induction by a similar range of environmental factorsincluding photoperiod and low temperature. It is likely that the MCDK (Martinez-Zapater, Coupland, Dean andKoornneef, 1994. In: Meyerowitz EM, Somerville CR. Arabidopsis. New York: Cold Spring Harbor Laboratory,403–433) model, formulated to explain the genetic and environmental control of flowering in Arabidopsis, could beemployed usefully in the formulation of experimental work on flowering in wheat and barley. This paper reviews theseissues, paying particular attention to the significance of ‘earliness per se ’ loci and the ‘constitutive floral pathway’for wheat and barley. # 1998 Annals of Botany Company

Key words : Wheat, barley, rice, Arabidopsis, flowering, photoperiod, vernalization, genetics, development.

INTRODUCTION

‘One of the major changes in plant science in the nextdecade will be in our way of approaching the problems. Inthe past we have taken a phenotype, which may be a processof response as well as a morphological feature, and haveattempted to gain understanding by perturbing conditionsin which we grow the plant. This approach has beenproductive but in general has not led us to an understandingof the basis and control of the process or structure’(Peacock, 1991).

The last 20 years have seen unprecedented interaction andcooperation among developmental biologists, environmen-

‡ For correspondence at : Scottish Agricultural Science Agency,East Craigs, Edinburgh EH12 8NJ, UK. E-mail hay!sasa.gov.uk

tal physiologists and mathematical modellers, resulting insubstantial advances in understanding of the biology ofagricultural species, and the development of a suite of cropsimulations (Thornley, 1990; Hanks and Ritchie, 1991).This has been particularly true of the temperate cereals,wheat (Triticum spp.) and barley (Hordeum �ulgare L.) : onthe one hand, the needs of modellers have stimulated thequantitative analysis of leaf and spikelet development,founded on the concept of the primordium as the unit ofdevelopmental progress (Hay and Kirby, 1991; Bossinger etal., 1992; Rickman and Klepper, 1995; McMaster, 1997)and, on the other, the resulting crop models are approachingthe stage at which they can be useful, for example inpredicting the effects of climatic change (e.g. Porter,Jamieson and Wilson, 1993; Hay, 1998).

Nevertheless, although valuable advances are still being

0305-7364}98}11054114 $30.00}0 # 1998 Annals of Botany Company

542 Hay and Ellis—Control of Flowering in Wheat and Barley

made in the 1990s (e.g. Wang et al., 1995a, b ; Evans andBlundell, 1996; Robertson, Brooking and Ritchie, 1996),conventional physiological approaches, whether field orlaboratory, have failed to answer some of the outstandingquestions about crop development posed by modellers [e.g.what determines the rate of development (the phyllochronor plastochron) for a given combination of cultivar andenvironment; what factors control the transition fromvegetative to reproductive development for non-adapted or‘non-standard’ cultivars?]. At the same time, the limitationsplaced upon crop simulation by gaps in understanding ofbasic biology are becoming increasingly obvious to cropmodellers (e.g. Ewert, Porter and Hornermeier, 1996).Faced with this impasse, it is important to ensure that allsources of relevant information are exploited, particularlycurrent developments in genetics and molecular biology(Devos and Gale, 1997; Yano and Sasaki, 1997).

The study of mutants has helped to establish the basicprocesses that occur at the stem apex. However, althoughBossinger et al. (1992) present a classic example of the useof mutants in barley to dissect the processes of plantdevelopment, it is notable that fewer than half of themutants have known loci. This indicates a gulf betweenclassical and mutation-based studies that is still to be filledby mapping with DNA-based markers. Another gap in theunderstanding exists between the role of genes determiningthe fate of cells at the apex, and those, for example, ofdaylength response and vernalization response genes, whichcontrol developmental rates and events. An indication ofthe importance to barley geneticists of studies in this area isgiven by the review of Hayes et al. (1997) which lists over 40mapping populations. Studies of the chromosomal locationof markers in these populations have been summarized inconsensus maps (Langridge et al., 1995; Qi, Stam andLindhout, 1996) and, in turn, these chromosome maps havebeen used to locate quantitative trait loci (QTL) including16 loci controlling heading date (Hayes et al., 1997).

The exploration of the molecular genetics of the Grami-neae has revealed evolutionary changes that are common tospecies as distinct as maize, Zea mays L., and rice, Oryzasati�a L. (Paterson et al., 1995) ; grasses started with asimilar ‘organisational plan’, which has been modified inthe process of domestication to promote useful cropcharacteristics (Fig. 3). The synteny between species of theTriticeae (such as barley and bread wheat, Triticum aesti�umL.) and O. sati�a is sufficient for direct comparisons of DNAsequences to be made (Dunford et al., 1995). Thus, theresults of many analyses of the smaller rice genome can betransferred to barley and wheat once syntenic relationshipsare established (Moore et al., 1995; Paterson et al., 1995;Sherman et al., 1995; Devos and Gale, 1997).

There have been relevant studies of the wild relatives ofcereal crop species. For example, within Hordeum, pheno-typic and genotypic analyses have shown that H. spontaneumC. Koch, the wild progenitor of H. �ulgare, is more diversethan modern crop cultivars (Nevo et al., 1997; Powell et al.,1997) ; and preliminary studies, at non-vernalizing tem-peratures, indicate that H. spontaneum shows a wider rangeof plant developmental responses than H. �ulgare (Kernich,Halloran and Flood, 1995a).

This paper reviews the physiology of barley and wheatdevelopment in the light of an overview of recent advancesin the conventional and molecular genetics of cereals andArabidopsis, which may provide clues to the control ofdevelopmental rate and the initiation of flowering.

DEVELOPMENTAL PHYSIOLOGY OFWHEAT AND BARLEY

E�ents at the stem apex

Field and laboratory measurements of the rate of initiationof primordia at wheat or barley stem apices (Hay andKirby, 1991; McMaster, 1997) have shown linear increasesin numbers with temperature, with the rate of spikeletinitiation higher than that of leaves. It is generally assumedthat the optimum for each is around 25–30 °C. Organo-genesis can, therefore, be described in terms of °C d abovethe appropriate temperature threshold, as shown for wheatin Fig. 1; the pattern for barley is broadly similar exceptthat a terminal spikelet is not formed, and only one floret isinitiated per spikelet (Kirby and Appleyard, 1987). Thereare few data on the modification of rates of primordiuminitiation by other environmental factors, although Kirbyand Ellis (1980) found that lower temperatures werecompensated for by longer daylengths, such that rates ofspikelet initiation were similar for English and Scottish sites(i.e. at different latitudes). This analytical approach empha-sizes the importance of the primordium, or the phytomer, asthe unit of development (Hay and Kemp, 1990; Bossinger etal., 1992).

The embryo of the mature caryopsis contains theprimordia of the first three or four leaves of the future main-stem (Kirby and Appleyard, 1987). Once germinationbegins, cell division restarts at the apices of the plumule andradicle (Georgieva et al., 1994) and initiation of primordiaresumes, such that two more leaves have been initiated bythe time that the first true leaf emerges through the coleoptile(i.e. full crop emergence: Growth Stage 10; Tottman andBroad, 1987). Crop emergence is more readily observedthan coleoptile emergence but it is important to emphasizethat the coleoptile, which responds to gravity (Edelman,1996) and low irradiance before emergence, will develop fullphototropic capability upon emergence (e.g. in maize; Liuand Iino, 1996). Coleoptile emergence is, therefore, likely toplay a role in setting the rate of primordium initiation. It isalso possible that primordium initiation is ‘pre-conditioned’during the early stages of embryo development on thedeveloping ear of the parent plant : for example, thecoleoptile of the rice embryo begins to form as early as 3±5 dafter anthesis and, by 8 d, the plumule apex is completelyenveloped by the coleoptile and leaves 1 and 2 (Suzuki et al.,1994).

Initiation of leaves proceeds regularly at intervals (plasto-chrons) of around 50 °C d (threshold 0 °C) for most wheatcultivars. The change to the initiation of floral primordia,the timing of which is determined by genotype}environmentinteractions (see below), in turn, determines the final numberof leaves produced by the main-stem. In the field, thisnumber normally varies from six to ten; with exceptionally

Hay and Ellis—Control of Flowering in Wheat and Barley 543

No. florets/spikelet

0Thermal time from sowing (degree days)

No.

leaf

an

dsp

ikel

et p

rim

ordi

a

40

20

Collar initiation(prim 13)

Terminalspikelet

(prim 32)

Florets

AnthesisSpikele

ts

Leaves

10

5

0

1No.

app

eare

d le

aves

(H

aun

) (

)N

o. le

aves

init

iate

d (

)

10

5

Flag leafinitiation

A

B

Flag leaf (12)appearance

Cropemergence

F. 1. Schematic diagram of the thermal time course of development of a model winter wheat plant (12 mainstem leaves, 19 spikelets per mainstemear, four grains per spikelet) including relationships between events : A, mainstem leaf initiation and appearance; B, mainstem leaf, spikelet andfloret initiation and death (note the change in scale for leaf initiation from A). The three apex stages illustrated are vegetative, ‘double ridge’ (here

around 50% spikelet initiation), and terminal spikelet (adapted from Kirby and Appleyard, 1987; Hay and Kirby, 1991).

early genotypes which are virtually insensitive to photo-period and have little or no vernalization requirement (e.g.a selection from cv. Sunset, Slafer and Rawson, 1995a ; theYunnan landrace Dianxiyangmai, Miao et al., 1992) finalleaf number per main-stem can be as low as five.

Although a bilinear pattern of organogenesis, withspikelets initiated at a higher rate than leaves, is charac-teristic of wheat and barley stems (tillers as well as main-stems), the point of inflection does not invariably coincidewith the initiation of the collar (i.e. the first reproductiveprimordium; Dele! colle et al., 1989; see also Evans andBlundell, 1996). Furthermore, the use of the ‘double ridge’stage as a sign of the switch from vegetative to reproductivedevelopment at the stem apex should be avoided as it does

not correspond to a precise stage in spikelet initiation (e.g.at 50–80% of spikelet initiation in wheat ; Dele! colle et al.,1989).

In most wheat and barley cultivars with a low vernali-zation requirement, the switch from producing leaves tospikelets occurs in response to long photoperiods. Since theplant can not respond to photoperiod until after coleoptileemergence, but the signal is transmitted from leaf to apex inhours rather than days, at least six leaves (exceptionally five,see above) will have been initiated by the main-stem apexbefore the collar can be initiated. Under such conditions,there is no indication that wheat or barley cultivarsexperience a significant juvenile phase (Roberts et al., 1988;Slafer and Rawson, 1994), as shown by rice and maize (see


below). The response to photoperiod is quantitative, andthe threshold and optimal photoperiods vary amongcultivars. Thus, although simulation of the influence of longphotoperiods on reproductive development of wheat orbarley main-stems is a relatively simple exercise, there is aneed for empirical input for each cultivar (Hay and Kirby,1991; Slafer and Rawson, 1994; Ewert et al., 1996).

Before they can respond to long days, the apices of mostwinter (and even some spring) cultivars must be vernalizedby a period of low temperature (or, for a minority ofcultivars, short days). Consequently, under inducing longphotoperiods, the initiation of the collar can be delayed, andthe number of leaves per stem increased, if the vernalizationrequirement has not been met. Vernalizing temperatures,unlike photoperiods, are experienced directly by apices, andthe critical number of degree days can be accumulated bythe embryo of the imbibed seed. Vernalization has been oneof the most poorly characterized aspects of cereal de-velopment, and modellers have had to rely on a smallnumber of data sets from a limited range of cultivars ; forexample wheat modellers have drawn heavily on pioneeringstudies of winter rye (e.g. Purvis, 1948).

Some of the difficulties arise out of isolating the progresstowards satisfying the vernalization requirement from otherconcurrent processes (Brooking, 1996; Robertson et al.,1996). Thus, for example, two apical processes (initiation ofleaf primordia and accumulation of the vernalizationrequirement), each influencing the final number of leavesper stem, are proceeding at the same time, but respondingdifferently to the prevailing temperature. Similarly, thetendency of higher (devernalizing) temperatures (possiblyfrom 20 °C upwards) to cause an increase in leaf number perstem acts in opposition to the steady progress to flowering,in the absence of inductive conditions; this appears to be afeature of all cultivars (response to endogenous signals, Hayand Kirby, 1991; see below for a discussion of ‘earliness perse ’ and the ‘constitutive floral pathway’). Using thisapproach, Brooking (1996) has recalculated the classicNorin 27 wheat data of Chujo (1966), to show that the rateof vernalization increased linearly between 1 and 11 °C. Thiswas, however, associated with an increase in leaf number permainstem (i.e. in determining the number of leaves per stem,the effect of increased temperature upon leaf initiation‘swamped’ its promotion of collar initiation). This analysis,which suggests that the effects of low temperatures (e.g. !5 °C) on vernalization have tended to be overemphasized,confirms the suggestion for barley that the optimumtemperature for vernalization could be as high as 10–12 °C(Trione and Metzger, 1970).

Another way of separating the effects of temperature ondevelopment in general from those on vernalization hasbeen to examine how the requirement for vernalizationdeclines with ontogeny (e.g. in spring wheats ; Jedel, Evansand Scarth, 1986). A more detailed study of winter wheatshas shown that, for example, seeds and 1-leaf seedlings ofwheat cv. Pioneer 2548 required at least 70 d at 5}2 °C tosatisfy their vernalization requirement, compared with 42 dat 4-leaf and 35 d at 7-leaf (Wang et al., 1995a).

Although it may prove possible to harmonize the resultsfrom these two methods of investigating vernalization

requirement, physiological approaches have yet to providea coherent model of the process of vernalization (Wang etal., 1995a). In part, this may be resolved by a betterunderstanding of the interactions between the accumulationof vernalization requirement and other processes such as theacquisition of frost hardiness (Hughes and Dunn, 1996;Sarhan, Ouellet and Vazquez-Tello, 1997).

Coordination of lea�es and ear

The interval between the appearance (emergence) ofsuccessive leaves of a stem (the phyllochron) is around twicethe (leaf) plastochron of the stem [ranging from 80 to200 °C d (threshold 0 °C), depending upon cultivar, locationand sowing date; Frank and Bauer, 1995]. It appears to beset at crop emergence, and generally remains constantthroughout canopy generation, although there are well-documented cases of the resetting of the rate of leafappearance during ontogeny, either around the time ofcollar initiation (e.g. Hay and Dele! colle, 1989) or during theappearance of the last few leaves (e.g. Hotsonyame andHunt, 1997; Slafer and Rawson, 1997). Such alterations inphyllochron may arise out of the coordination of phyllo-chron and plastochron, since leaf initiation is controlled bytemperature whereas the rate of spikelet initiation is alsoinfluenced by photoperiod, and there may also be a changein base temperature (Hay and Kirby, 1991; Slafer andRawson, 1995c ; see also Kernich, Halloran and Flood,1997; Slafer and Rawson, 1997).

The extension of stem internodes, and the resultingappearance of the ear, are closely coordinated with leafappearance, such that the appearance of the flag leafinvariably occurs shortly before heading (Hay and Kirby,1991). Consequently, the number of days to heading can beexpressed in terms of two (plant) variables : the number ofleaves initiated and the rate of leaf appearance (or thephyllochron). The factors determining the number of leavesinitiated by a stem (temperature, photoperiod) have beenconsidered in the previous section. Although it has provedpossible to predict the phyllochron of certain standardwheat cultivars in terms of the rate of change of daylengthat crop emergence, the relationship is not general and is notsupported by the results of field and laboratory experimentsin which daylength has been artificially manipulated (Kirby,1995; Kernich, Slafer and Halloran, 1995b ; Hotsonyameand Hunt, 1997; McMaster, 1997).

What the physiologist does not know about thede�elopment of wheat and barley

This brief review of the interaction between developmentalphysiology and modelling has shown that there are majorgaps in our knowledge in two important areas. First, it is notknown what determines the ‘rate of development’ (plasto-chron or phyllochron) of a given cultivar at a given locationand sowing date, including both genotype effects andgenotype with environment interactions. Secondly, althoughthere is considerable knowledge of the temperature relationsof vernalization, and of threshold and optimal photoperiods,understanding of the initiation of reproductive development


200

200

Days to heading (not vernalized, short days)

Day

s to

hea

din

g (v

ern

aliz

ed, l

ong

days

)

100

180

160

140

120

80

60

40

20

20 40 60 80 1000 120 140 160 180

Spring

Winter

F. 2. Relationships between days to heading under conditions favouring floral induction (vernalization requirement satisfied, 16 h photoperiod)and days to heading under non-inductive conditions (vernalization requirement not satisfied, natural short days) for 81 spring (D) and 36 winter

(*) wheat cultivars grown in a glasshouse in Canberra, Australia (from data of Davidson et al., 1985).

is primitive (e.g. Ewert et al., 1996). For example, little isknown about the processes which eventually bring aboutcollar initiation in the absence of inductive conditions.Linking these two areas is the unexplained and verysubstantial variation in time to heading of cultivars heldunder inductive conditions (e.g. Fig. 2). It is the thesis of thisreview that progress in these areas will come from moderngenetics (see Ellis, 1993).

THE APPROACH OF THE GENETICIST}PLANT BREEDER TO THE DEVELOPMENT

OF WHEAT AND BARLEY

Work on the physiology and modelling of the reproductivedevelopment of cereals tends to concentrate upon a fewcultivars, with the aim of compiling a detailed phenotypicdescription of a given genotype. This can form thefoundation for a comprehensive model (e.g. AFRC-WHEAT2 is constructed largely from measurements ofAvalonwinterwheat and related genotypes), and subsequentcomparison with other cultivars. However, because of alack of knowledge about the genetic control underlyingphenotypic expression, these studies do not give insight intoplant reaction to environments outside the original modelenvironments. These limitations are reflected in the con-clusions drawn by Wilson, Russell and Ellis (1991) that : (1)‘ limiting the expression of genotype to its effects on phasicdevelopment, as in the ARCWHEAT Model, despite theknock-on effects on canopy development and assimilatepartitioning, oversimplifies reality and prevents distinctionbetween cultivars ’ ; and (2) ‘ the CERES Model assumptionthat the genetic specific coefficients are constants overdiverse environments remains unproved, since the inter-

action effects are obscured by large errors in modelling ofcanopy development and biomass accumulation’.

In contrast, geneticists and plant breeders have ap-proached the genetic control of traits and processes bystudying the allelic �ariation among genotypes. Barley, as aninbred diploid, and one of the five most important cropspecies, has been the subject of many genetical analyses,particularly because of the ease of creating and studyingmutants (Nilan, 1991). Many mutants have been isolated,and mapped using morphological, isozyme and physio-logical markers, as illustrated by Franckowiak (1994).Developmental mutants have been isolated with changes in:pattern of tillering (cul2 ; Kirby, 1973), time of heading(eam8 ; Yasuda, 1977), vernalization requirement (sgh, Sgh2,Sgh3 ; Takahashi and Yashuda, 1971) and stem morphology(ert series ; Persson, 1969). In contrast to physiologicalmodelling, knowledge of the genotype facilitates the pre-diction of responses such as heading date in environmentswhere temperature and photoperiod vary.

In the study of quantitative traits (which include mostdevelopmental traits), the geneticist is looking for easily-identified phenotypes or genotypes, and simply does nothave the time to dissect plants to determine the stage ofapical development (Kernich et al., 1995b). For practicalreasons, therefore, ‘flowering’, ‘awn emergence’ and ‘head-ing’ (appearance of the ear above the flag leaf), are regardedas synonymous, and progress to reproductive developmentis quantified in terms of ‘days to heading’ or ‘days toanthesis ’ normally from sowing date, but also occasionallyfrom crop emergence.

In view of the complex series of coordinated processeswhich culminate in ear emergence (e.g. Fig. 1 ; Hay andKirby, 1991), it is necessary to draw a clear distinction


between the number of genes}QTL that may be involved inthe processes from sowing to ear emergence (clearly many),and the number of genes whose effects can be detected in theanalysis of heading-time data. For example, in modernbarley cultivars with the sdw1 short-straw gene, thepleiotropic effect of this gene obscures the action of others(Thomas, Powell and Swanston, 1990). An improvedstrategy is to use stepwise experimentation, in whichgenotypes representing the extremes of the populationdistribution are identified and then studied in greater detail :in one study, Nandi et al. (1997) started with 250 randominbred lines but continued with 74 from each extreme of thepopulation to map genes for tolerance to submergence inrice.

In summary, the geneticist’s approach to a trait such asheading must be statistical, and involves evaluation of theprobability that a given genetic locus is active in the controlof a trait or process. There are continual improvements instatistical technique (Hackett, 1997) but marker}traitassociation and its use in breeding programmes is an areathat still requires further research.

THE MAPPING OF GENES INVOLVED INDEVELOPMENT

Quantitati�e traits and QTL

Days to heading is a quantitative trait : an unknown numberof genes is involved, each with the ability to segregate andrecombine, but there is also the possibility of epistasis (onegene influencing the effect of another) and pleiotropy (onegene affecting more than one trait). In addition, the patternof gene expression can vary with location (genotype withenvironment interactions) (Falconer and Mackay, 1996).Each of this suite of genes (or each set of tightly-linkedgenes at a locus on a chromosome) is a quantitative traitlocus (QTL).

Progress in understanding the genetic (and ultimately thephysiological) control of a quantitative trait necessitates theidentification and mapping of the relevant QTL (Laurie,Snape and Gale, 1992). This involves locating markers, forwhich the genotypes are readily scored, on each chromo-some, and estimating the ‘distance’ between QTL andmarkers in terms of the frequency of recombination betweenthem following controlled crosses (Staub, Serquen andGupta, 1996). [The resulting units of distance, centiMorgans(cM), do not relate to physical distance or numbers of basepairs, and can vary between locations on chromosomes;Lee, 1995; Griffiths et al., 1996.] The mapping of headingdate and height on chromosome 4(4H) of barley by Hackettet al. (1992) is an example of QTL analysis using more‘traditional ’ isozyme and morphological markers, but thedevelopment of molecular markers brought about a rev-olution in gene mapping for quantitative traits. Tinker(1996) at http:}}www.css.orst.edu}research}Barley}qtl}qtltitle.htm (‘New strategies for QTL mapping’) gives anexplanation of QTL mapping in seminar format. Of equalimportance has been the availability of computer packagesfor the treatment of complex data sets of markers andquantitative traits, including ‘MAPMAKER’ (Lander et

al., 1987), ‘GMendel ’ (Holloway and Knapp, 1994) and‘MQTL’ (Tinker and Mather, 1995).

Mapping wheat genes using aneuploidy

At first sight, bread wheat might appear to be a very poormodel system for genetic analysis. As a hexaploid (2n¯ 6x¯ 42) with three sets of homoeologous chromosome pairs(genomes AABBDD) apparently inherited from threedifferent ancestor species, it has the potential to carry atleast six doses of each allele. [Durum wheat, Triticum durumL., is a tetraploid (2n¯ 4x¯ 28) with two sets of homoeo-logous chromosome pairs (genomes AABB)]. This com-plicates analysis owing to the considerable potential forepistasis. On the other hand, this genetic buffering permitsthe wheat genome to function normally in the absence ofone or more chromosomes, in the absence of chromosomearms, as well as with additional or substituted chromosomesfrom other genotypes and related species (Islam, Shepherdand Sparrow, 1981; Law, Snape and Worland, 1987; Devosand Gale, 1993). Comparison of the phenotype of suchaneuploids or substitution lines with the unaltered euploidcan reveal the chromosome on which a gene or QTL islocated, and measurement of recombination with markergenes can give information at least about the arm on whichit is located. (Wheat}barley addition lines can, of course,also reveal the positions of loci on barley chromosomes.)

This approach to gene mapping is extraordinarily labo-rious, involving the skilled preparation of full series ofaneuploids with each chromosome lost, reduced in size orsubstituted from another genotype (Sears, 1954; Snape,1987). Nevertheless, by the mid-1980s, genetic analysis ofheading date using wheat aneuploids had revealed thepresence and approximate position of four major genes forinsensitivity to vernalization (Vrn1, Vrn2 and Vrn3, on thelong arms of 5A, 5B and 5D, respectively; and Vrn5, shortarm 7B) and two (or three) major genes for insensitivity tophotoperiod (Ppd1, Ppd2 and, possibly, Ppd3 on the shortarms of 2D, 2B and 2A, respectively) (Table 1). As discussedbelow, studies of this kind, generally in collaboration withphysiologists, also indicated a range of further genetic lociinfluencing heading date (e.g. Miura and Worland, 1994),and the great potential for genotype with environmentinteractions (e.g. Redden, 1991).

Mapping wheat and barley quantitati�e trait loci usingmolecular markers

Progress on the mapping of QTL has accelerated in barleyin particular (Laurie et al., 1992; Thomas et al., 1995;Powell et al., 1997; Waugh et al., 1997), but also in wheat,with the increased availability of molecular markers, initiallymaking use of restriction fragment length polymorphism(RFLP) (Paterson, Tanksley and Sorrels, 1991). Later workhas made use of other marker systems, including randomamplified polymorphism (RAPDs) and amplified fragmentlength polymorphism (AFLPs) (Laurie et al., 1992, 1995;Hayes et al., 1993, 1997; Staub et al., 1996; Tinker et al.,1996; Karsai et al., 1997), and microsatellites are likely tobecome more important. The results of these analyses are


T 1. Major genes controlling date of heading in wheatand barley (Law et al., 1987; Worland et al., 1987; Laurie et

al., 1994; Worland, 1996; Laurie, 1997)

Gene Chromosome}Arm Comment

Wheat (T. aesti�um)Ppd1Ppd2Ppd3

2D}short2B}short2A}short

5

6

7

8

Recessive alleles (ppd)confer photoperiodsensitivity (need for long days).

Effectiveness 1" 2" 3

Vrn1Vrn2Vrn3

5A}long5B}long5D}long

5

6

7

8

Recessive alleles (vrn)confer vernalizationsensitivity (need for lowtemperature).

Vrn3 most effective.Vrn5 7B}short

Barley (H. �ulgare)Ppd-H1 2(2H)}short Dominant allele confers

photoperiod sensitivity

sgh (sh)Sgh2 (Sh

#)

Sgh3 (Sh$)

4(4H)}long7(5H)}long5(1H)}long

5

6

7

8

Winter alleles confervernalization sensitivity.

Interactions occur among loci.Winter allele required at allloci for strong vernalizationsensitivity.

estimates of the probability that the magnitudes of thetrait}s are influenced by different loci on the chromosomes(e.g. which loci on the chromosomes are active in deter-mining days to heading) ; the accuracy of the location of lociof statistical significance, measured in cM from the originalmarkers, depends upon the spacing between markers. Usingpresent technology, the error in placing a locus on a wheator barley chromosome will be of the order of 5–20 cM,which can represent tens of thousands of base pairs,depending upon the amount of repetitive DNA in thatregion of the chromosome (Lee, 1995; Staub et al., 1996).

Molecular mapping, and associated analysis of aneu-ploids, have shown that a wide range of genes and loci areinvolved in the determination of days to heading oftemperate cereals (at least 20 in wheat and 16 in barley:Laurie et al., 1995; Worland, 1996; Hayes et al., 1997). Inaddition to the major vernalization and photoperiodsensitivity genes (Table 1), a number of subsidiary vernali-zation and photoperiod loci, and what are loosely termed‘earliness per se ’ loci, have been detected in each species (onchromosomes 2B, 2D, 3A, 4A, 4D, 6B, 6D and 7B in wheat ;Worland, 1996; on 1(7H), 2(2H), 3(3H), 4(4H), 6(6H) and7(5H) in barley; Laurie et al., 1995). For barley, thesignificant pleiotropic influence of the major stature genesdw1 (syn. swd1 ; denso) in delaying heading (e.g. Laurie etal., 1995), needs to be interpreted in terms of thecoordination of leaf appearance, stem extension and earemergence (Fig. 1). In general, these findings complementthe findings of purely physiological investigations, althoughinterest has recently focused on ‘earliness per se ’ locibecause they may be involved in setting rates of development(e.g. Slafer and Rawson, 1995b ; see below).

At the present accuracy of mapping loci in wheat and

barley, it is difficult to isolate and clone individual genes.However, in view of the modest size of the rice genome (430million base pairs : around 1}30th the size of that of wheat),the degree of homoeology which appears to exist within theGramineae (Fig. 3; see below), and the present rapid rate ofsequencing and mapping the rice genome, it seems likelythat the next phase of progress in the understanding ofheading of cereals will come from rice (Yano and Sasaki,1997). However, while waiting to evaluate the usefulness ofinformation from rice, one more conventional approachcould be deployed more widely : the study of the physiologyof isogenic lines, which has proved very useful in revealingthe functions of Rht genes (e.g. Flintham et al., 1997).

HOMOEOLOGY IN THE GRAMINEAE

As molecular mapping of wheat, barley, maize, rice andother grasses progressed during the 1990s, it becameapparent that, in relation to single copy genes, there isextensive conservation of gene order among species ; thisoccurs in spite of the considerable variation in chromosomenumber, and in the amount of intergenic (largely repetitive)DNA which has accumulated since speciation (e.g. Naranjoet al., 1987; Whitkus, Doebley and Lee, 1992; Ahn andTanksley, 1993; Kurata et al., 1994; Devos, Moore andGale, 1995; Paterson et al., 1995). Subsequent comparativemapping has shown that if the rice genome (which is thesmallest grass genome under active study) is considered interms of 19 or 20 ‘ linkage blocks ’ or ‘segments ’, rather thanentire chromosomes, then the genomes of seven taxa of theGramineae can be aligned in a set of concentric circles (Fig.3). There will shortly be sufficient information to includefurther species such as pearl and finger millets, and perennialryegrass. Allowing for some irregularity caused by trans-location and duplication, markers common to six species,and members of the Triticeae (wheats, barley, rye), arefound on corresponding arcs. This has led to the concept ofan ancestral Gramineae genome similar to that of modernrice, possibly in the form of a single chromosome (Moore etal., 1995).

The relationships shown in Fig. 3 provide powerful toolsfor advancing the understanding of many physiologicaltraits, not least flowering in cereals. In terms of photoperiod-sensitivity genes, it was already known that the Ppd-H1 geneon the short arm of chromosome 2(2H) of barley waslocated in a similar position to the Ppd genes on the shortarms of each of the group 2 chromosomes of wheat. It isnow possible to show that these wheat and barley genesalign with a region of rice chromosome 7 which carries amajor QTL, Hd-2, for date of heading, and the photoperiodresponse gene se2 is also present on chromosome 7 (Laurie,1997). Corresponding photoperiod-sensitivity loci have alsobeen established for maize and sorghum (Paterson et al.,1995).

At present the picture is less clear for vernalization-sensitivity genes. The Sgh2 (Sh

#) locus of barley [long arm,

7(5H)] corresponds to the Vrn (long arm, group 5) and Sp1loci of wheat and rye, respectively, but loci corresponding tosgh1 (sh) and Sgh3 (Sh

$) have not been established (Laurie,

1997). Since low-temperature vernalization is not required


F. 3. Alignment of the genomes of six major grass crop species with 19 linkage segments of rice, whose order may reflect a common ancestralgrass genome. The Triticeae (wheats, barleys, rye) are represented by the D genome of the bread wheat variety Chinese Spring. A full explanationof the chromosome codings can be found in Devos and Gale (1997). (Reproduced with the kind permission of Kluwer Academic Publishers.)

for the flowering of rice, comparative mapping of this traitoffers less potential at present ; ultimately it may be possibleto identify the genes which have been altered to give Vrn,Sgh (Sh) and Sp loci (or those which have lost this role). Thedata on ‘earliness per se ’ loci are still too uncertain to allowthe appropriate comparisons.

In the case of photoperiod-sensitivity genes, comparativemapping is reaching the level of precision at which, becauseof the much smaller genome of rice, the accurate identifi-cation and sequencing of genes, for example by genewalking (Griffiths et al., 1996), becomes a possibility. Oncea particular gene has been isolated then the existence andlocation of corresponding genes on the chromosomes ofothermembers of theGramineae (Fig. 3) can be investigated,for example using cDNA probes. However, it is alreadyclear that full exploitation of the results of such geneticanalysis will depend upon understanding the comparativephysiology of the species ; for example, how do homoeo-

logous photoperiod-sensitivity alleles from different speciesoperate in contrasting ways, causing an acceleration ofheading in response to longer or shorter days in wheat,barley and rice cultivars adapted to different environments(Laurie, 1997). The issues of juvenility in rice and maize,and its absence in practice in most temperate cereal cultivars ;and the basic differences between members of the Gramineaein terms of development (e.g. spike �s. panicle ; Bossinger etal., 1992; and the separation of tassel and cob in maize),must also be considered.

Progress in isolating photoperiod-sensitivity genes may,however, be even more rapid, as a result of work on otherspecies with even simpler genomes. The isolation andcharacterization of the CONSTANS (CO) gene family,whose role in Arabidopsis closely parallels that of Ppd inwheat (Laurie, 1997), suggests that extensive homoeologymay span the monocot}dicot divide, although comparativemapping is somewhat hampered by differences in codon


usage across the divide (Hughes, 1996). The genetic controlof flowering in Arabidopsis and other dicots is discussedbelow.

RATE OF PLANT DEVELOPMENT ANDEARLINESS PER SE

Taking days to heading as an index, there are basicdifferences in rate of development between winter andspring cultivars ; depending upon the interaction betweenthe environment and need for vernalization and}or ap-propriate photoperiod, the date of heading can differ byseveral weeks. Where the need for vernalization has beenmet early in development, the exposure of plants to highly-inductive photoperiods can result in very different headingdates. For example, most of the 117 wheat cultivars treatedin the glasshouse in this way by Davidson et al. (1985)headed in 40–60 d, but around 10% (all winter types)required more than 100 d, and the highest value exceeded200 d (Fig. 2). This indicates that there are intrinsicdifferences in the rate of development between cultivars (i.e.in their ‘earliness ’) which must have a genetic basis, eventhough the time to heading in a given environment can varywith temperature (Slafer and Rawson, 1995b).

This study also showed that under non-inductive con-ditions, without prior vernalization, all cultivars dideventually head (Fig. 2), at times varying between 50 and190 d, and that there was a broad relationship between thetwo heading dates for each cultivar (e.g. late cultivars werelate under both sets of conditions). The winter types dideventually initiate reproductive development in the absenceof vernalization and without being exposed to what wouldbe considered to be a threshold photoperiod for flowering.

170

505

Leaf number at anthesis

Ph

yllo

chro

n, °

C d

per

leaf

110

130

150

90

70

7 9 11 13 15

8 h non-vernalized

16 h vernalized

F. 4. Relationships between the mainstem phyllochron and leaf number at anthesis for 20 spring wheat cultivars grown under conditionsfavouring floral induction (vernalization requirement satisfied, 16 h photoperiod; *) and non-inductive conditions (vernalization requirement notsatisfied, 8 h photoperiod; D) in a glasshouse at ICARDA, Syria (from data of Mosaad et al., 1995). Note that the values for two pairs of cultivars

coincided under 16 h (at 6±2 leaves}102 °C d and 7±6 leaves}102 °C d).

Under such circumstances, it is possible that the signal forcollar development is the initiation of a certain number ofleaves, or achievement of a certain apical volume}shootsize, as found in a range of contrasting species (Poethig,1990; Manupeerapan et al., 1992). Other evidence, however,suggests that progress to reproductive development hasbegun before this stage: Wang et al. (1995a, b) haveconfirmed that the need for vernalization declines pro-gressively with ontogeny, and subsequent work (U. Schul-thess, pers. comm.) has indicated that the thresholdphotoperiod declines in the same way. Thus progress toreproductive development can be seen to be an integralcomponent of ontogeny (the concept of a ‘constitutive floralpathway’ e.g. Zagotta et al., 1992) which can accelerate inresponse to environmental cues.

If the phyllochron remains constant or near-constantfrom crop emergence to flag leaf appearance, earlier headingcan be the result of fewer leaves (earlier initiation of thecollar), faster leaf appearance, or a combination of the two.There is a wealth of information on the variation in main-stem final leaf number among different cultivars held underthe same conditions (e.g. reviewed by Hay and Kirby, 1991;see also Fig. 4). Comparable information on the phyllochronof different cultivars held under the same conditions isscarcer ; where variation has been demonstrated, it hasnormally been substantially less than the variation in leafnumber (e.g. Cutforth, Jame and Jefferson, 1992; Frankand Bauer, 1995; Kernich et al., 1995b ; Hotsonyame andHunt, 1997). Nevertheless, in a glasshouse experiment inSyria (Mosaad et al., 1995) which examined 20 contrastingspring wheat cultivars, some of which did require vernali-zation, the least inductive treatment (8 h, no prior vernali-zation, 22 °C day}18 °C night) revealed very substantial


differences between cultivars, the highest main-stem phyllo-chron value being nearly 60% higher than the lowest (Fig.4). Significant differences were established across the fullrange of cultivars, although 14 did fall within the interval110 to 130 °C d per leaf (at final leaf numbers varying fromeight to 15). By contrast, under the most inductive treatment(16 h day, prior vernalization, same temperatures), 18cultivars had values between 90 and 110 °C d, at final leafnumbers between six and eight (Fig. 4).

Earliness in wheat and barley is, therefore, largelyassociated with low final leaf numbers rather than shorterphyllochrons, although there are cultivars which showvariation in phyllochron which is of a comparable scale tothat shown by final leaf number (e.g. Fig. 4). This tends tosuggest that interpretation of the role of ‘earliness per se ’genes in wheat and barley should concentrate upon theireffects on collar initiation and mainstem leaf number,including the progress to reproduction without induction(for example, in extremely early photoperiod-insensitivecultivars ; Gallagher, Soliman and Vivar, 1991), rather thanon possible effects on phyllochron. Advances in this areamay well have to wait until detailed information is availableon the ‘earliness per se ’ genes which are known forArabidopsis (see below). Nevertheless, it will be important toinvestigate the report that ‘a single major gene may controlthe phyllochron in some cultivars (of rice) ’ (Nemoto,Morita and Baba, 1995).

THE INDUCTION OF FLOWERING INARABIDOPSIS THALIANA

Arabidopsis thaliana has proved to be an ideal model speciesfor the exploration of the molecular basis of plant processes.It has a small genome (120 million base pairs, around onequarter of the size of the rice genome) with relatively fewrepeat sequences, making it possible to search for genes bymethods such as gene walking and gene tagging (Smyth,1990). Its life cycle is short (around 6 weeks), it is self-fertile,undemanding in its growing conditions, and the small sizeof the plants facilitate large glasshouse experiments. These,and other factors played an important part in the choice ofA. thaliana as the primary higher plant species for completegenome sequencing.

Progress in studying the genetics of flowering, in Australia,Germany, the UK and the USA, has been particularly rapidbecause of the existence of a wide range of viable floralmutants of Arabidopsis (in addition to a wide range of otherdevelopmental mutants). A great deal is now known aboutthe genetic control of floral meristem identity, and thesubsequent development of floral organs (Coen, 1991;Meyerowitz and Somerville, 1994; Weigel, 1995; Ma, 1998) ;this work is beyond the scope of this review. However, workon mutants with widely-varying flowering times has alsorevealed that at least 20 loci are involved in the induction ofreproductive development (Weigel, 1995; Table 2). Theseinclude genes controlling responses to daylength (both longand short days, and associated signalling by phytochrome)and low temperature vernalization; genes involved withflowering response to the presence or absence of growthsubstances (gibberellin, abscisic acid, ethylene) ; and a

T 2. Flowering-time genes from Arabidopsis (collatedby Weigel, 1995)

Gene Symbol

Late flowering

CONSTANS CODE-ETIOLATED 2 DET2ETHYLENE INSENSITIVE 2 EIN2ETHYLENE RESISTANT 1 ETR1FRIGIDA FRI¯FLAGIGANTEA GILATE FLOWERING FCA, FD, FE, FHA,

FLC, FPA, FT, FVE,FWA, FY

LUMINIDEPENDENS LDVERNALIZATION INSENSITIVE VRN

Early flowering

EARLY FLOWERING 1–3 ELF1, ELF2, ELF3EMBRYONIC FLOWER 1, 2 EMF1, EMF2LONG HYPOCOTYL 1, 2 HY1, HY2PHYTOCHROME B PHYBSPINDLY SPYTERMINAL FLOWER TFL

Late flowering in short days only

GIBBERELLIN INSENSITIVE GAIGIBBERELLIN REQUIRING 1 GA1

Early flowering in short days only

ABSCISIC ACID DEFICIENT ABAABSCISIC ACID INSENSITIVE ABI1

Not delayed by short days

CONSTITUTIVEPHOTOMORPHOGENIC 1

COP1¯FUSCA1

DE-ETIOLATED 1 DET1¯FUSCA2

Night-break}daylength—extension insensitive

PHYTOCHROME A PHYA

diverse group of genes of less defined function (i.e. ‘earlinessper se ’ genes). In most of this work ‘flowering’ has beenrecorded in terms of time to the opening of the first flower,or time to the appearance of the first stigma (i.e. analogousto time to heading in cereals) ; few studies have involvedmore quantitative measures of development such as numberof leaves initiated by the apex (Martinez-Zapater et al.,1994).

Martinez-Zapater et al. (1994) have now organized thesevarious flowering time responses into an ingenious andcoherent model (the MCDK model) for the control offlowering time in Arabidopsis (Fig. 5 ; Table 2). The modelrelies upon the existence of one or more floral repressors (asyet unidentified) whose effect can be reversed in severalways, resulting in the initiation of flowering. These include:exposure to long days, signalled via PHYA, leading to theaction of a suite of genes including CO ; and low-temperaturevernalization which stimulates the expression of VRN,whose effect is transmitted via a suite of genes controllingthe level of growth substances, notably gibberellins. In thescheme, short-day repression of flowering, signalled viaPHYB, occurs through the action of a suite of genes on thesignalling function of growth substances. In addition to


constitutivepromotion

FRI, LD, FCA, FLC,FPA, FVE, FY

vernalizationVRN

GA signalingGA1, GAI, SPY,ABA, ABI1

GA signaling

FLORALREPRESSOR

LD promotion

CO, GI, FD, FEFHA, FT, FWA

constitutiverepression

TFL, ELF1,2 (ELF3,PHYB, HY1,2?)

DET1,COP1 PHYA

REPRODUCTIVE PHASEVEGETATIVE PHASE

ELF3, PHYB,HY1,2

SD repression

F. 5. The MCDK model of the control of flowering time in Arabidopsis, indicating some of the participating genes (see Table 2). The arrowheads signify promotion, the blunt heads repression, and the repression of a repression gives promotion (from Weigel, 1995). (Reproduced, with

permission, from the Annual Re�iew of Genetics, Volume 29 # 1994 by Annual Reviews.)

these environmentally-modulated effects the model allowsfor flowering without induction by a constitutive pathway,including both promotion and repression, and involvingmany of the ‘earliness per se ’ genes.

This model is the first attempt at a coherent explanationof the full range of factors influencing flowering inArabidopsis, and its main roles will be in the planning offuture experimental work, and in the interpretation ofresults. Nevertheless, the many similarities in the control offlowering of Arabidopsis and of temperate cereals (daylengthsensitivity, vernalization requirement, the role of gibberellinsand stature genes, and the occurrence of flowering withoutenvironmentally-modulated induction), also mean that thismodel could well be applied to the planning and in-terpretation of flowering experiments in cereals.

Understanding of the control of floral induction inArabidopsis is advancing rapidly. For example, manipu-lation of the expression of the flowering-time gene CO hasrevealed its roles in activating floral meristem-identity genes(i.e. establishing the link between the induction of re-production and the subsequent development of floralorgans) (Simon, Igeno and Coupland, 1996; Ma, 1998) ; andthe first steps have been taken in characterizing themechanism of constitutive promotion of floral induction(Macknight et al., 1997). Other work has revealed that theprocess of vernalization involves the demethylation, andtherefore the availability for transcription, of stretches ofDNA (Peacock, 1991; Ronemus et al., 1996). Dependingupon the degree of homoeology which can be establishedbetween Arabidopsis and rice, for example, it is only amatter of time before we have much more detailedunderstanding of the control of heading in cereals, and thephysiological processes involved.

ACKNOWLEDGEMENTS

RKMH is grateful to the Scottish Office Agriculture,Environment and Fisheries Department (SOAEFD) forstudy leave in North America in 1997. This review arose outof discussions and correspondence with numerous scientistsin Edinburgh, Norwich, Dundee, Montreal, E Lansing,Guelph and Orange NSW. Their contributions are gratefullyacknowledged, although they are in no way responsible forthe way in which their ideas have been incorporated intothis paper. SCRI is grant-aided by SOAEFD. Dr M. D. Galekindly provided the original for Fig. 3.

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