Evolution of physiological responses to salt stress in hexaploid wheat

Abstract

Hexaploid bread wheat (Triticum aestivum L., genome BBAADD) is generally more salt tolerant than its tetraploid wheat progenitor (Triticum turgidum L.). However, little is known about the physiological basis of this trait or about the relative contributions of allohexaploidization and subsequent evolutionary genetic changes on the trait development. Here, we compared the salt tolerance of a synthetic allohexaploid wheat (neo-6x) with its tetraploid (T. turgidum; BBAA) and diploid (Aegilops tauschii; DD) parents, as well as a natural hexaploid bread wheat (nat-6x). We studied 92 morphophysiological traits and analyzed homeologous gene expression of a major salt-tolerance gene High-Affinity K + Transporter 1;5 (HKT1;5). We observed that under salt stress, neo-6x exhibited higher fitness than both of its parental genotypes due to inheritance of favorable traits like higher germination rate from the 4x parent and the stronger root Na + retention capacity from the 2x parent. Moreover, expression of the D-subgenome HKT1;5 homeolog, which is responsible for Na + removal from the xylem vessels, showed an immediate transcriptional reprogramming following allohexaploidization, i.e., from constitutive high basal expression in Ae. tauschii (2x) to salt-induced expression in neo-6x. This phenomenon was also witnessed in the nat-6x. An integrated analysis of 92 traits showed that, under salt-stress conditions, neo-6x resembled more closely the 2x than the 4x parent, suggesting that the salt stress induces enhanced expressivity of the D-subgenome homeologs in the synthetic hexaploid wheat. Collectively, the results suggest that condition-dependent functionalization of the subgenomes might have contributed to the wide-ranging adaptability of natural hexaploid wheat.transcriptional rewiring | Na + homeostasis | salinity tolerance P olyploidy or whole genome duplication (WGD) is a pervasive, driving force in plant and vertebrate evolution, which has fascinated biologists for more than a century (1, 2). The common occurrence of WGD suggests an evolutionary advantage of having multiple genomes at least in certain circumstances, which might have enabled the polyploid organisms to be better adapted to some adverse environmental conditions than their diploid progenitors (3, 4). Polyploidy can instantaneously develop novel features that allow them to invade new territories or expand their parental niche (3). Polyploids may also exhibit higher evolvability than their diploid progenitors, which allows them to adapt to capricious environmental conditions (4). Thus, polyploidy has been demonstrated as a process that may lead to saltational speciation especially when novel ecological niches are available for colonization.Although abrupt genome duplication often produces adverse effects on physiology at both cellular and organismal levels (4, 5), it has been shown that polyploidy in plants may result in favorable physiological consequences such as increased photosynthetic capacity and enhanced tolerance to biotic and abiotic stresses, which ...

Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat

“…A notable observation is the substantial differences among the normal chromosomes in their responses to a given whole-chromosome aneuploidy, which have accumulated to marked differential responses by the three subgenomes, with subgenome B being significantly more responsive than subgenomes A and D. This is consistent with the findings that the three subgenomes of hexaploid wheat are asymmetric at both structural and expression levels (Feldman et al, 2012;Pont et al, 2013) and are functionally partitioned across development or under different environmental conditions (Pfeifer et al, 2014;Yang et al, 2014). Notably, subgenome expression asymmetry in polyploid wheat is already evident at the onset of allopolyploidization, which showed further augmentation in the course of evolution and domestication at both the tetraploid and hexaploid levels .…”

Gene Duplicability of Core Genes Is Highly Consistent across All Angiosperms

“…Indeed, increasing evidence suggests that polyploids show wider environmental tolerance and higher levels of phenotypic plasticity than diploids ( Van de Peer et al, 2009b;Hahn et al, 2012;te Beest et al, 2012;Yona et al, 2012;Chao et al, 2013;Vanneste et al, 2014b;Selmecki et al, 2015;Sunshine et al, 2015). In particular, transporters and metabolic genes, enriched in the "multicopy" class, have been identified before as putative driver genes explaining the increased tolerance of polyploids for environmental stress (Dunham et al, 2002;Selmecki et al, 2006Selmecki et al, , 2015Gresham et al, 2008;Yang et al, 2014;Sunshine et al, 2015). Despite the strong correlation between gene duplicability and gene function observed here, it remains to be further investigated which evolutionary mechanisms are responsible for the observed strong bias in duplicate retention patterns, and it remains to be established whether gene function directly influences gene duplicability or whether biased gene retention could be a by-product of other evolutionary phenomena instead, such as for instance the preservation of intermolecular interactions (dosage balance) or sequence constraints related to high levels of gene expression (Davis and Petrov, 2004;Drummond and Wilke, 2008).…”

Making the Bread: Insights from Newly Synthesized Allohexaploid Wheat

“…Polyploids allow experiments to be conducted that are not possible in diploids and the insights gained can be incorporated into modified models to explain heterosis at all levels (Washburn and Birchler, 2014). Newly synthesized wheat allohexaploids indeed exhibits certain hybrid vigor and adaptive traits as mentioned earlier (He et al, 2003;Colmer et al, 2006;Yang et al, 2014). Moreover, the tractable genetic pedigree and high ploidy of synthetic wheat should provide special values in studying the molecular basis of polyploid heterosis.…”

“…Nascent hexaploid wheat exhibits certain hybrid vigor and adaptive traits, such as robust seedling growth, larger spikes, and salt tolerance when compared with the parents (He et al, 2003;Colmer et al, 2006;Yang et al, 2014). Morphologically, nascent hexaploid wheat is more similar to that of T. turgidum in plant height and spike shape, while the longer rachis internodes seem to be inherited from the paternal progenitor Ae.…”