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Plant Stems: Physiology And Functional Morpholo...



Polyploidy is well studied from a genetic and genomic perspective, but the morphological, anatomical, and physiological consequences of polyploidy remain relatively uncharacterized. Whether these potential changes bear on functional integration or are idiosyncratic remains an open question. Repeated allotetraploid events and multiple genomic combinations as well as overlapping targets of artificial selection make the Brassica triangle an excellent system for exploring variation in the connection between plant structure (anatomy and morphology) and function (physiology). We examine phenotypic integration among structural aspects of leaves including external morphology and internal anatomy with leaf-level physiology among several species of Brassica. We compare diploid and allotetraploid species to ascertain patterns of phenotypic correlations among structural and functional traits and test the hypothesis that allotetraploidy results in trait disintegration allowing for transgressive phenotypes and additional evolutionary and crop improvement potential.




Plant Stems: Physiology and Functional Morpholo...


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Among six Brassica species, we found significant effects of species and ploidy level for morphological, anatomical and physiological traits. We identified three suites of intercorrelated traits in both diploid parents and allotetraploids: Morphological traits (such as leaf area and perimeter) anatomic traits (including ab- and ad- axial epidermis) and aspects of physiology. In general, there were more correlations between structural and functional traits for allotetraploid hybrids than diploid parents. Parents and hybrids did not have any significant structure-function correlations in common. Of particular note, there were no significant correlations between morphological structure and physiological function in the diploid parents. Increased phenotypic integration in the allotetraploid hybrids may be due, in part, to increased trait ranges or simply different structure-function relationships.


Polyploidy is well studied from a genetic and genomic perspective, but the morphological, anatomical, and physiological consequences of polyploidy remain relatively uncharacterized; datasets are necessary for a comprehensive understanding of the formation and persistence of polyploids as well as their evolutionary and agroecological implications [30]. Repeated allotetraploid events and multiple genomic combinations as well as overlapping targets of artificial selection make the Brassica triangle an excellent system for exploring variation in the connection between plant structures (anatomy and morphology) and function (physiology) as well as studying the effects of artificial selection and polyploidy. We use a panel of Brassica triangle species to ask whether repeated allopolyploid events that generated B. carinata, B. juncea, and B. napus result in altered trait expression and trait correlations. Specifically, we ask whether structural aspects of morphology and anatomy are correlated with functional physiology and test the hypothesis that allotetraploidy results in disintegration of phenotypic trait correlations allowing for transgressive phenotypes and additional evolutionary and crop improvement potential.


As a conservative approach to ensure that significant results do not derive from the effects of one or two data points, all data were subjected to an outlier analysis. Data points for each plant and trait outside three standard deviations of the grand mean (calculated including all individuals from all species) were excluded. Subsequent visual inspection of histograms and quantile-quantile plots indicated that excluding two data points for F o ' and three for F m ' and F s improved normality. Significant effects of species and ploidy (2n vs. 4n) were assessed using a series of one-way ANOVAs with planned contrasts for individual species effects and the effect of ploidy level (i.e. parent vs. hybrid species) in the R statistical environment (v3.2.3, [38]). We dropped all traits that lacked significant species or parent-hybrid effects from further analyses (except the principle components analysis, below). We used log-transformed data from individual plants to calculate phenotypic correlations for all six species, parents, and hybrids while using a Bonferroni correction for multiple tests (cor.test). We interpret correlations that are observed only in the parents as evidence that the history of selection has resulted in functional integration at the phenotypic level and that hybridization has broken down these trait correlations. We interpret correlations only observed in the hybrids as evidence that novel allelic combinations arising from allopolyploidy has the potential to generate new phenotypic correlations not observed in parent species.


Physiological function such as light gathering and harvest are critical to plant survival and reproduction. Many of these processes occur within leaves, where the ability to maintain hydraulics, conduct gas exchange, regulate temperature, harvest light, and dissipate excess light energy are dependent on leaf anatomic and morphological structures. Given the complex and multifaceted roles leaves play, one expectation is that leaf morphological and anatomical structures should be highly integrated with leaf-level physiological function. One of the most obvious examples of leaf structure-function relationship is kranz anatomy in C4 plants, where specialized bundle sheath and mesophyll cells surround vascular bundles and provide improved separation and improved efficiency of carboxylation and decarboxylation reactions [41]. Leaf-level structure-function relationships are also evident in larger datasets that include both C3 and C4 plants [42]. However, studies of the relationship between leaf structure and function often examine only morphological aspects of leaves, such as specific leaf area or leaf thickness, rather than internal anatomical variation among leaves (e.g. [42]). From a functional perspective, internal anatomy may be much more directly related to physiological processes, including gas exchange and carbon assimilation rates than external morphology [43]. Further, evolutionary diversification and crop improvement can be constrained by trait correlations [44, 45]. Genomic doubling, specifically allopolyploid formation may break down phenotypic trait correlations, leading to phenotypic instability and opening up new potential targets for natural and artificial selection [4, 46]. We examine phenotypic trait correlations among structural aspects of leaves including external morphology and internal anatomy with leaf-level physiology among several species of Brassica. We compare diploid parental species with allotetraploid hybrids and ascertain that patterns of phenotypic integration among structural and functional traits change after large-scale genomic reorganization such as the occurrence of polyploidy.


Suites of traits governing similar aspects of organismal biology are often highly integrated. In rice, structural aspects of leaves such as leaf thickness and mesophyll cell surface area are highly inter-correlated while functional aspects of leaves such as photosynthetic rate and stomatal conductance are also highly inter-correlated [54]. However, phenotypic integration is not a forgone conclusion; recent work in tomato reveals relatively weak coordination between leaf structure and function [55]. We identified three intercorrelated suites of traits in both diploid parents and allotetraploids. Morphological traits such as leaf areas and perimeters were significantly correlated (Figures S1-S3). Anatomic traits were also correlated such as ab- and ad- axial epidermis areas (Figures S1-S3). Finally, aspects of physiology were correlated including F o ', F v ', and Fs (Figures S1-S3), likely because these values are all mechanistically related to photosystem II function. However, correlations between suites of structural traits (morphological and anatomical) were also present. For instance, SLA was correlated with the ratio of palisade parenchyma to spongy mesophyll (Figure S3). Palisade parenchyma typically consists of densely packed cells compared to the relatively large extracellular air spaces in spongy mesophyll, explaining why leaves with a high SLA would also have a higher ratio of palisade parenchyma to spongy mesophyll. Leaf area and perimeter were correlated with spongy mesophyll area (Figures S1 and S2). Spongy mesophyll tissue, which has large extracellular spaces may be less costly to construct than more densely packed palisade parenchyma and so scales more directly with leaf area, particularly for larger leaves [56].


We examined multiple accessions from each of three allotetraploids and their functionally diploid parent species in the classical Brassica Triangle of U to test if leaf structure-function relationships, many of which are highly conserved across the leaves of seed plants, can change after hybridization. Novel genomic combinations and interactions allow for the break down of ancestral phenotypic trait correlations and the generation of novel trait correlations not exhibited by the parent species. Genomic and chromosomal instability in early generation allotetraploids may allow these species to explore new trait space and potentially reach higher adaptive peaks than their progenitor species could, despite temporary fitness costs [68]. The trait correlations that disappear after hybridization as well as the novel trait correlations observed in allotetraploid Brassica hybrids may represent relatively evolutionarily labile associations and therefore could be ideal targets for artificial selection and crop improvement.


The role of the potato stem in drought tolerance has hardly been studied, even though the stem plays vital and indispensable roles in the bidirectional transport of water, photo-assimilates, and other products of metabolism, with the vascular tissues of the stem, xylem, and phloem, mediating the transport processes (Gartner 1995). The stem is also a potential reserve water pool to maintain leaf water potential in functional boundaries (Banik et al. 2016; Lechthaler et al. 2016). The stem xylem which consists of tracheids (narrow tubes with tapered ends) and vessel members that make up the vessel (wider tubes but shorter than tracheids and joined end-to-end), transports water and nutrients from the soil to different plant parts. Xylem transport is driven by transpiration and, therefore, operates under negative pressure, and it involves various stem components (Holbrook and Zwieniecki 2011; Tyree and Zimmermann 2013). 041b061a72


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