Aquatic Botany 122 (2015) 47–53

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Aquatic Botany

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Typha domingensis Pers. growth responses to leaf anatomy andphotosynthesis as influenced by phosphorus

Karina Rodrigues Santos, Marcio Paulo Pereira, Ana Carolina Goncalves Ferreira, LuizCarlos de Almeida Rodrigues, Evaristo Mauro de Castro, Felipe Fogaroli Corrêa,Fabricio José Pereira ∗

Universidade Federal de Lavras, Departamento de Biologia, Campus Universitário, Lavras, State of Minas Gerais 37200-000, Brazil

a r t i c l e i n f o

Article history:Received 7 July 2014Received in revised form 23 January 2015Accepted 27 January 2015Available online 29 January 2015

Keywords:CattailEutrophicationEcological anatomyEcophysiology

a b s t r a c t

Cattail (Typha domingensis Pers.) can show intense growth depending on phosphorus (P) eutrophication.We verify how P enrichment and deficiency influence T. domingensis growth and the relationship withanatomical and physiological modifications. Vegetative T. domingensis plants were grown for 60 days ina modified nutrient solution in five P levels: 0, 0.20, 0.40, 0.60 and 0.80 mM. Plant growth was evaluatedat the end of the experiment. Leaf fragments were collected and fixed in F.A.A.70 and sectioned in bench-top microtome. Sections were stained with safrablau solution, mounted in slides and photographedwith an optical microscope. Images were evaluated in UTHSCSA-Imagetool software which was usedto measure leaf tissues. Leaf gas exchanges were evaluated 30 and 60 days after the experiment started.The data were submitted to one-way ANOVA and regression analyses or means were compared usingthe Scott–Knott test. Plants showed more growth in a P-rich nutrient solution. T. domingensis showeddifferent biomass partitioning under P levels, with an increasing leaf biomass allocation for higher P levelsand a lower rhizome investment. For higher P levels, plants showed increased photosynthesis, stomatalconductances and transpiratory rates. However, the highest concentration promoted a decrease in thesecharacteristics. The leaves of T. domingensis showed larger stomata, thicker palisade parenchyma and anincreased phloem proportion under higher P levels. Our results suggest that the increased growth of T.domingensis in P-rich conditions may be related to increased photosynthesis; this characteristic is limitedto anatomical traits such as palisade parenchyma and stomatal modifications.

© 2015 Elsevier B.V. All rights reserved.

1. Introduction

Typha domingensis Pers. (Typhaceae), is a native species in SouthAmerica and it may show intense vegetative expansion colonizingwide areas (Martins et al., 2007). T. domingensis may be importantto the animals living in these environments (Silveira et al., 2012)and in phytoremediation (Hegazy et al., 2011).

Uncontrolled growth of T. domingensis has been reported tobe the result of phosphorus (P) enrichment of the environment(Newman et al., 1998; Li et al., 2010), notably in the everglades.This P enrichment may lead to the decline of previously dominantnative species. As an example, Macek et al. (2010) reported thealmost-complete reduction of the Eleocharis spp. population whencompeting with T. domingensis in nitrogen- and P-rich environ-

∗ Corresponding author. Tel.: +55 3538291616; fax: +55 3538291341.E-mail address: fabriciopereira@dbi.ufla.br (F.J. Pereira).

ments. Miao et al. (2000) also described the increased populationgrowth of T. domingensis under P enrichment. At the same time,T. domingensis may be important for P removal from P-rich envi-ronments as it has been used in constructed wetlands for thispurpose (Chen and Vaughan, 2014). However, Escutia-Lara et al.(2009, 2010) reported no responses to P enrichment in T. domin-gensis growth.

There have been few studies concerning the anatomical char-acteristics of T. domingensis. Henry (2003) described the leaves ofT. domingensis showing stomata on both the adaxial and abaxialsurfaces and sclerenchyma fibers between palisade parenchymagroups. Likewise, monocotyledon plants of some species experienc-ing P deficiency show poorly developed leaf tissues (Kavanová et al.,2006). Physiological traits in T. domingensis are poorly understoodbut Miao et al. (2000) reported higher photosynthetic potential inT. domingensis plants growing in P-rich environments. Likewise,previous studies have described that anatomical leaf modifica-tions such as higher mesophyll thickness and stomatal number

http://dx.doi.org/10.1016/j.aquabot.2015.01.0070304-3770/© 2015 Elsevier B.V. All rights reserved.

48 K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53

can be related to increased photosynthesis (Nikolopoulos et al.,2002; Pereira et al., 2011). Therefore, the differences between T.domingensis growth responses in previous studies may be relatedto different anatomical (stomatal and chlorophyll parenchyma inleaves) and physiological (photosynthetic rate) adaptations of thisspecies under different P levels. We aim to verify how P enrichmentand deficiency influence T. domingensis growth and the relationshipwith anatomical and physiological modifications.

2. Experimental

2.1. Plant materials and experimental design

T. domingensis plants were collected in the southeastern regionof Brazil in Alfenas, Minas Gerais State, 21◦25′44′′S, 45◦56′49′′W,from natural wetlands. Plants collected in environment comprisedof rhizomes (25 cm length and 3 cm of diameter) and about tenleaves. The plants were washed with tap water and grown in agreenhouse in a nutrient solution (Hoagland and Arnon, 1940) at40% ionic strength for 60 days to obtain acclimatized clone plants.

The clone plants were standardized according to size (rhi-zomes showing about 15 cm length) and number of leaves (aboutfive leaves), all clone plants were at the same age and in thevegetative stage. There were no inflorescences or new clones inplants used in experiment. Plants were placed in polypropylenevases (38 × 53 × 8 cm) containing 4 L of modified nutrient solu-tion at 20% ionic strength with increasing P levels (0.0, 0.2, 0.4,0.6 and 0.8 mM). The experiment was carried out under theseconditions for 60 days and nutrient solution was replenished in15 days intervals, nutrient levels was monitored with handheldcondutivimeter (Mettler–Toledo, Greifensee, Switzerland). There-fore, plants at the end of the experiment were 120 days oldand showed no inflorescences remaining at the vegetative state.Phosphorus levels in P-rich environments are reported for someBrazilian wetlands such as the 1800 �g P g−1 water as reported byBorges et al. (2009) and Canadian hypertrophic wetlands may reach0.2 mM P (White et al., 2000). Likewise, Steinbachová-Vojtískováet al. 2006 considered 0.999 mM a hypertrophic concentration forphosphorus and Wang et al. (2013) state that 25 mg L−1 is anextremely high phosphorus level. Therefore, we classify the 0.6and 0.8 levels as P-rich environments and 0.2 and 0.0 mM of P asP-poor solution. The nutrient solution comprised from concentra-tions described by Hoagland and Arnon (1940) using the followingsalts: NH4H2PO4, Ca(NO3)2, Mg(NO3)2, KNO3, K2SO4, FeSO4·7H2O,H2BO3, MnSO4·H2O, ZnSO4·7H2O, CuSO4·5H2O, H2MoO4·H2O.

The experimental design was completely randomized with fivetreatments and six replicates and the parcel constituted of one plantfor each replicate.

2.2. Growth evaluation

Growth evaluation was performed by measuring the leaves,roots and stem dry mass on an analytical balance at the end ofthe experiment. Dry mass was obtained by drying the plant partsin an oven at 45 ◦C for 48 h. Leaf area was measured at the end ofthe experiment by photographing the leaves and measuring theirarea using UTHSCSA-Imagetool software (The University of TexasHealth Science Center, San Antonio, Texas, USA). The physiologicalgrowth indices were calculated as described by Hunt et al. (2002)and the relative growth rate (RGR) and the leaf area ratio (LAR) wereobtained. The net assimilation rate (NAR) was obtained by multi-plying (RGR × LAR). Biomass partitioning was calculated for eachorgan by dividing its dry mass by the entire plant dry mass; theresults were expressed as a percentage (%). Expansion was assessed

by counting new shoots each day and the final number of shoot foreach replicate was calculated after 60 days.

2.3. Anatomical evaluation

For the anatomical analysis, fragments in the middle of fullydeveloped leaves were fixed in a solution of formaldehyde, aceticacid and 70% ethanol (F.A.A. 70) for 72 h and then stored in 70%ethanol until further analysis (Kraus and Arduin, 1997). Paradermalleaf sections were obtained using steel blades on both the abax-ial and adaxial surfaces and the sections were cleared with 50%sodium hypochlorite, rinsed in distilled water twice for 10 min,stained with 1% aqueous safranin, and mounted on slides with50% glycerol (Johansen, 1940). Cross sections were obtained at themiddle leaf region and root maturation zone using the LPC model(Behringer, Belo Horizonte, Brazil) bench-top microtome. Sectionswere cleared with 50% sodium hypochlorite, rinsed twice in dis-tilled water for 10 min, stained with safrablau solution (1% safraninand 0.1% astra blue in a 7:3 ratio) and mounted on slides with 50%glycerol. The slides were photographed using a BX 60 model (Olym-pus, Tokyo, Japan) with a digital camera (Canon A630; Canon Inc.,Tokyo, Japan). For each replicate, we evaluated five sections andfive fields for each section.

UTHSCSA-Imagetool software was used for image analysis. Wemeasured the following parameters: NSaD = number of stomataper field, NCaD = number of epidermal cells per field, POLaD = polardiameter of the stomata, SEDaD = equatorial diameter of the stom-ata, SDaD = stomatal density (stomata per mm2), PERaD = stomatalratio between POL/EQU, SIaD = stomatal index, NSaB = numberof stomata per field, NCaB = number of epidermal cells perfield, POLaB = polar diameter of the stomata, SEDaB = equatorialdiameter of the stomata, SDaB = stomatal density (stomata permm2), PERaB = stomatal ratio between POL/EQU, SIaB = stomatalindex, AbE = abaxial epidermis thickness, AdE = adaxial epidermisthickness, MF = mesophyll thickness, PPaD = palisade parenchymathickness from adaxial side, PPaB = palisade parenchyma thick-ness from abaxial side, SP = spongy parenchyma thickness, PP/SPratio = palisade and spongy parenchyma ratio, DV = distancebetween vascular bundles in the mesophyll, BSC = diameter of thebundle sheath cells and PAE = proportion of aerenchyma gaps inthe leaves (area/area).

2.4. Gas exchange evaluation

We evaluated the leaf gas exchange characteristics using aninfrared gas analyzer (IRGA), LI-6400XT model (Li-COR Biosciences,Lincoln, Nebraska, USA). The gas exchange evaluation was per-formed twice at 30 and 60 days after the beginning of theexperiment and two fully expanded leaves were evaluated for eachreplicate. The evaluation started at 10 am. and the photosyntheticphoton flux density (PPFD) was fixed at 1000 �mol m2 s−1 in thedevice chamber. Thus PPFD was chosen from previous light satu-ration tests to these plants and to avoid photoinhibition or a lackof radiation. We additionally evaluated the stomatal conductance(gs), transpiration rate (E), photosynthetic rate (A) and the ratiobetween internal and external carbon (Ci/Ca).

2.5. Statistical analysis

The data were subjected to MANOVA and principal componentanalysis (PCA) was performed previous to F test and multiple com-parison analysis. PCA was performed in order to select the mostsignificant variables among our data. Eigenvalues were used tohighlight significant factors. All factors showing Eigenvalues of 1.0or higher were assumed as significant. Factors were added to obtain85% or higher values for explained variability. Significant variables

K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 49

Fig. 1. Growth characteristics of T. domingensis cultivated at different P levels in the nutrient solution. The bars correspond to the standard errors. Means followed by lettersin panel D do not differ according to the Scott–Knott test at p ≤ 0.05.

were selected to F test and multiple comparisons of means, how-ever, previous to F test, data was subjected to Shapiro–Wilk testfor normal distribution and Lavene test for variance homogeneity.Statistical significance was presumed for p < 0.05 and regressionanalysis was conducted. Principal component analysis was per-formed in Statistica software and F test as well as regressionanalysis was preformed using Sisvar statistical software.

3. Results

Higher P concentrations promoted more vegetative growth. At60 days, T. domingensis plants exposed to higher P concentrationshad produced more new plants proportional to the P level in thenutrient solution (Fig. 1A). Phosphorus also increased the biomassproduction of each plant, leading to plants at least three times largerthan plants grown in the solution lacking P (Fig. 1B). Higher P levelsalso accounted for differences in plant biomass partitioning in dif-ferent plant organs. As shown in Fig. 1C, T. domingensis decreasedthe biomass allocated to rhizomes but increased its investment inleaf production with increasing P levels.

Net photosynthesis increased in T. domingensis plants exposedto higher P levels in the nutrient solution. Plants showed higherphotosynthetic rates until a P level of 0.4 mM in the solution; thephotosynthetic rates dropped in the higher concentrations tested(0.8 mM), as shown in Fig. 2A. Likewise, the stomatal conduc-tance increased with increasing P levels until the 0.4 mM solution;reduced conductances were observed in higher concentrations(Fig. 2B). A very similar result was observed in the transpiration,which showed increasing values until the 0.4 mM level and reducedmeans in the plants exposed to higher P levels (Fig. 2C).

Paradermal sections of T. domingensis leaves reveal stomata onboth the adaxial and abaxial sides. Stomata show two bean-shapedguard cells as well as two parallel subsidiary cells on both sidesof the longer stomatal axis. Epidermal cells show many differ-ent shapes and very straight cell walls that lack sinuosities. Thestomata are randomly distributed along the surface on both sidesof the leaves. Quantitative analysis revealed no modifications tothe equatorial diameter (Fc = 1.32, p = 0.26; mean = 10.81 �m) and

stomatal density (Fc = 2.41, p = 0.49 and mean = 452 stomata mm−2)on the leaves’ abaxial sides. However, P promoted anatomical mod-ifications on most of the evaluated traits on the leaves’ abaxialsides. Increasing P levels promoted larger stomatal polar diame-ters (Fig. 3A), a higher polar-to-equatorial diameter ratio (Fig. 3B)and an increased stomatal index (Fig. 3C). Likewise, the stomatalratio between the polar and equatorial diameters increased withhigher P concentrations (Fig. 3D), as did the stomatal index (Fig. 3E).However, the stomatal density showed no changes with P concen-trations (Fc = 2.00; p = 0.09) and was characterized by an average of423 stomata mm−2.

The thickness of the epidermis from both leaf sides was notmodified by the P level (Fc ≤ 0.866, p ≥ 0.48); the mean epidermisthickness from the abaxial side was 12.62 �m and 12.34 �m for theadaxial side. The palisade parenchyma thickness of the abaxial sideshowed no changes induced by P level (Fc = 0.61, p = 0.65), showingan average value of 84.23 �m. However, the palisade parenchymafrom the adaxial side was increased with P concentration in thenutrient solution but was reduced for higher P levels (Fig. 3F). Theleaf vascular bundles of T. domingensis from both the adaxial andabaxial sides showed increased phloem areas proportional to theapplied P level (Fig. 3G). However, the xylem proportion on the vas-cular bundles from the adaxial side decreased with P concentration(Fig. 3H) and showed no modifications on the abaxial side (Fc = 1.86,p = 0.12, mean = 20.32%).

T. domingensis leaves in transversal sections revealed a thinsingle-layered epidermis on both the abaxial and adaxial sides(Fig. 4). Three cell layers of palisade parenchyma were found closeto the epidermis of the abaxial and adaxial sides (Fig. 4). Betweenthe palisade parenchyma layers, large spongy parenchyma areaswere found showing big aerenchyma gaps (lacunae). Collateralvascular bundles containing xylem and phloem were distributedamong the palisade parenchyma on both leaf sides. These vascularbundles have fibers and a bundle sheath comprising parenchyma(Fig. 4). This leaf structure was observed in all P treatments; thenumber of cell layers of tissues, as well as the arrangement of cells,was not modified by the P levels tested. Even plants grown for60 days in the solution lacking P exhibited well-developed tissues

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Fig. 2. Leaf gas exchanges of T. domingensis cultivated at different P levels in the nutrient solution. The bars correspond to the standard errors.

on both their adaxial and abaxial sides (Fig. 4A and F), althoughdifferences in cell size were evident in some tissues (Fig. 4).

4. Discussion

Higher plant growth is often reported for plants exposed to Penrichment such as Potamogeton crispus (Wang et al., 2013) andeven T. domingensis (Li et al., 2010; Macek et al., 2010). However,Escutia-Lara et al. (2010) reported no modifications to T. domin-gensis growth with varying P enrichment. We observed increasedvegetative growth and individual biomass production in T. domin-gensis promoted by P enrichment in the nutrient solution. Thisfinding is very similar to of the results of previous works reportedin the literature. However, discrepant results in the literature maybe related to P concentration because, as will be discussed later,physiological and anatomical modifications in higher P levels mayhelp to explain the differences observed in previous studies.

We found a clear modification in biomass partitioning of T.domingensis related to P level. Since roots are important for P uptakeand are produced by T. domingensis rhizomes, low P levels pro-moted a higher rhizome allocation of biomass. This fact may leadto a larger number of roots for P uptake. This result may be related toan increased number of thinner roots that are more efficient at tak-ing up nutrients (Roose and Fowler, 2004; Simunek and Hopmans,2009).

Increased P levels promoted higher leaf biomass allocation onT. domingensis, leading to larger photosynthetic areas and higherplant and population growth. The shoot biomass of T. domingensiswas evaluated by Escutia-Lara et al. (2010), who found no impactof P level on this trait. However, when grown under eutrophic andhypertrophic conditions when all macronutrients were enriched,T. angustifolia showed a larger biomass allocation to shoots anda larger number of leaves (Steinbachová-Vojtísková et al., 2006).Natural environments showing higher P levels promoted highergrowth rates and leaf biomass allocations in T. domingensis plants(Miao et al., 2000). In fact, Grace and Wetzel (1981) attributedthe larger capacity to growth and competition of T. latifolia to T.angustifolia due to its broader leaves which developed a largerphotosynthetic area. Despite divergent data reported by previous

studies, we found that T. domingensis can increase its biomass allo-cation to leaves under higher P levels in the nutrient solution; thiseffect may be related to a larger leaf area useful for photosynthesisand enhanced plant growth.

Balemi (2009) reported no modification, or even reduced netphotosynthesis, in potato plants depending on genotype. In fieldconditions, Miao et al. (2000) found increased photosynthesis forT. domingensis plants growing in P-rich sites. Stress conditionsmay limit the net photosynthesis of T. domingensis; Chen andVaughan, 2014 reported lower photosynthesis for T. domingen-sis plants exposed to higher inundation depth, which decrease Puptake in plants. We found reduced photosynthesis levels for bothlower and higher P levels. This fact suggests that P deficiency alonedoes not limit T. domingensis photosynthesis, but some other addi-tional factor may be related to the higher levels of photosynthesis.

According to Zhou and Han (2005), the two factors that limitphotosynthesis are light and CO2 availability. Therefore, reducedstomatal conductance values and transpiration with higher P lev-els in T. domingensis leaves suggest that higher P levels promotestomatal limitations to CO2 uptake, reducing photosynthesis. Sto-matal data support this statement because we found larger stomatain plants growing in higher P concentrations but reduced stomatalsizes in highest P concentration. Since stomata are related to CO2uptake and may improve photosynthesis under stress conditions(Pereira et al., 2011), larger stomata may be related to larger areasfor gas exchange, enhancing photosynthesis.

Shen et al. (2006) postulated that P plays a role in signaling sto-matal development related to the calcium network in Arabidopsisthaliana. We found an increased stomatal index in T. domingensisleaves exposed to higher P levels but no changes in stomatal den-sity. This finding may be related to the larger stomata producedby P enrichment, which took up more room on leaves, leading to asimilar stomatal density even with more stomata developing fromthe protodermis. This result supports the hypothesis that P playsa role in stomatal development, increasing the stomatal numberin P-rich conditions. This response is important to T. domingensisthereby promoting increased CO2 uptake and photosynthesis.

Another important anatomical trait in T. domingensis that wasmodified by P enrichment was palisade parenchyma thickness.

K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 51

Fig. 3. Anatomical leaf characteristics of T. domingensis cultivated under different P levels in the nutrient solution. A–E: stomatal characteristics; F–H: tissue characteristicsat transverse sections. A–C: abaxial side; D–E: adaxial side. The error bars indicate standard errors. The error bars correspond to standard errors.

Cell elongation of some monocotyledon leaves such as Loliumperene may be limited to low P availability (Kavanová et al.,2006). Chiera et al. (2002) reported thinner palisade parenchymain soybean leaves under P stress. Therefore, a P limitation mayexplain the lower palisade parenchyma thickness in nutrient solu-tions lacking this element. However, the palisade parenchymathickness was strongly reduced in plants growing in P levels of 0.6and 0.8 mM. A larger leaf thickness is related to an enhanced pho-tosynthesis potential (Shipley et al., 2005), which may be relatedto the larger size of chlorophyll parenchyma. Likewise, the pho-tosynthetic limitation on T. domingensis in both higher and lowerP conditions may also be related to the reduction of palisadeparenchyma thickness.

Increased phloem development may be an important character-istic of stress tolerance by enhancing plant growth capacity (Pereiraet al., 2011). Furthermore, an increased phloem proportion may berelated to the larger growth to T. domingensis in a P-rich solutionbecause this tissue is responsible for the transport of photosynthe-sis products to sink organs.

Despite all of the anatomical improvements caused by higher Plevels, another important result we observed was the capacity of T.domingensis to develop functional leaves even in solutions lackingP. As reported by Chiera et al. (2002), leaves in low-P solutionsshowed poorly developed tissues, even after only 16 days of P stress.We observed that T. domingensis leaves showed well-developedleaf tissues after 60 days of P stress. This result indicates a strong

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Fig. 4. Transverse sections of T. domingensis leaves cultivated under different P levels in the nutrient solution. A–E: abaxial side of the leaves; F–J: adaxial side of the leaves. Aand F = 0.00, B and G = 0.20, C and H = 0.40, D and I = 0.60 and E and J = 0.8 mM of P in the nutrient solution. gp = ground parenchyma, pp = palisade parenchyma, ep = epidermis,vb = vascular bundle, x = xylem, p = phloem. The scale bars correspond to 100 �m.

K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 53

tolerance for P stress; T. domingensis develop as smaller plantsbut show functional organs only with the P stored in rhizomes.All of our results suggest that T. domingensis growth is enhancedby higher P levels and that this increase is related to photo-synthesis and anatomical improvements. However, our findingsare dependent on the P concentration in the nutrient solution,leading to the findings distinct from those reported in previousstudies.

Therefore, T. domingensis growth is dependent of P concen-tration as follows: low P levels reduce growth by limiting leafproduction and photosynthesis; in despite excess P also limitsphotosynthesis. This clearly shows a limit for P efficiency on T.domingensis growth. This may be related to contrasting results inprevious works (Miao et al., 2000; Escutia-Lara et al., 2010; Li et al.,2010) because experiments under low or too high P levels may leadto similar effects. Likewise, the photosynthesis limitation in low orexcess P levels is related to anatomical modifications in palisadeparenchyma and stomata in leaves.

Acknowledgements

The authors thank CNPq (Conselho Nacional de Desenvolvi-mento Científico e Tecnológico [National Counsel of Scien-tific and Technological Development], CAPES (Coordenacão deAperfeicoamento de Pessoal de Nível Superior [Coordination forthe Improvement of Higher Education Personnel]), and FAPEMIG(Fundacão de Amparo à Pesquisa do estado de Minas Gerais[Minas Gerais State Research Support Foundation]) for funding andresearch grants awarded to complete the present study.

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