Metabolic Changes of Legume Polyploids with Salinity Stress: History
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Phetole Mangena

Salinity stress affects plant growth and development by causing osmotic stress and nutrient imbalances through excess Na+, K+, and Cl− ion accumulations that induce toxic effects during germination, seedling development, vegetative growth, flowering, and fruit set. However, the effects of salt stress on growth and development processes, especially in polyploidized leguminous plants, remain unexplored and scantly reported compared to their diploid counterparts.

  • antioxidant activity
  • autopolyploidy
  • genome duplication
  • legumes

1. Physiological and Molecular Status of Leguminous Polyploids

In legumes, polyploidy serves as a major genetic driver in regulating growth and development processes, including the legume-rhizobium symbiosis, which plays an important role in the global nutrient cycle and diversification of plant species, as previously mentioned [1]. Accordingly, such interactions may have further consequences that include differential expression of common and distinct gene families depending on the strength and activity of promoter sequences. Some of these expressed genes may encode proteins that are responsible for significant notable physiological and phenotypic changes that enhance the resistance of leguminous plants to abiotic stresses such as salinity, drought, and high temperature. However, at this molecular level, salinity influences the expression of genes related to the biochemical parameters associated with salt tolerance. For instance, in non-leguminous species, such as Steria rebaudiana Bertoni (an important medicinal plant native to northeastern Paraguay and southern Brazil), the overexpression of peroxidase encoding genes (POD4, POD6, and POD9) was reported [2].
The expression of these genes virtually influenced all metabolic reactions and physiological processes, specifically the functional pathways, nutritional imbalances, and hormonal regulations, eventually getting all these impeded. Although, unlike the widely reported drought-triggered effects on gene regulation and expression, the effects of salinity are more physiologically pronounced, involving major biochemical metabolite synthesis, enzyme induction, and membrane transport than the upregulation and downregulation of plant genes. If mineral ions (Na+, Cl−, and K+) in the soil are in excess, such conditions will inhibit plant growth by interfering with plant cell osmotic adjustment and then reduce ROS scavenging activity through specialized enzymes and antioxidants [3]. Razzaque et al. [4] reported allelic diversity at several genetic loci that have been found in genotypes that show tolerance to an excess of these salt-stress-inducing ions (Na+, Cl− and K+), influencing the growth and nutritive value of leguminous crops. However, the marked physiological effects in polyploids because of genome doubling and altered gene functions revealed increased adaptability to environmental variability [5]. Genome duplication may lead to the improvement and/or divergence of an entire duplicated pathway, among others, resulting in noticeable changes in the physiological traits related to water use efficiency and photosynthesis. Such alterations include those of chlorophyll and hydrogen peroxide contents, together with abscisic acid (ABA), which were regarded as physiological indicators to judge the response of polyploidized L. ruthenicum plants against environmental stress [6]. Under reduced soil water content, which also led to osmotic stress from dehydration, the diploids showed inhibition of chlorophyll synthesis and an excessive increase in the concentration of hydrogen peroxide (H2O2). The superoxide dismutase produced H2O2 gets increased during environmental stress, interacting with thiol-containing proteins and activating the different signaling pathways, including transcriptional factors (TFs) involved in the regulation of gene expression and cell-cycle processes in plants.

2. Ionic and Osmotic Stress Signaling Responses in Polyploidized Plants

To cope with salinity stress, plants have developed several adaptive strategies, such as enhanced enzymatic and physiological reactions, as well as higher levels of metabolite expression, such as phenols that are involved in the antioxidant activities of the plant. This stress affects vital metabolic functions whereby Na+ and Cl− ions interfere with several nutrients. Salt stress affects competitive nutrient uptake, accumulation, and transport in plants [7], consequently disturbing nutritional balance and hormone interactions, causing osmotic stress effects and specific ion toxicity [8]. In soybean, the ratio of gibberellin (GA) and abscisic acid (ABA) was negatively regulated by NaCl during seed germination and post-germinative growth [9].
In terms of inorganic ions, essential elements (N, P, K, S, Mg, etc.) are considered intrinsic components of the structure and metabolism in plants [10][11]. The severe abnormalities that may arise due to salinity stress will result in symptoms of specific nutritional deficiencies such as chlorosis and necrosis. It remains common knowledge that salt stress influences the transfer of inorganic nutrients from the environment into a plant [12], but further insights are still required on how nonspecific osmotic stress and specific ion effects are regulated at both physiological and molecular level. Even though, the mechanisms through which legumes with altered ploidy adapted to salinity stress still need to be investigated, insights on other non-leguminous crops demonstrated novel traits and changes in existing physiological processes because of polyploidization.
As previously reported, polyploidized mutants always showed improved biosynthetic, carbolic, and signaling transduction pathways under environmental stress. In the general scheme of signal transduction, polyploidized plants would likely show rapid environmental and developmental signal perception by specialized receptors and effective activation of a signaling cascade involving secondary messengers, leading to an efficient response by the plant cells [4][13]. Part of polyploids’ success is signaling between plants and microbes during symbiotic nitrogen fixation (SNF), which influences microbial infection of plant cells, cell division leading to nodulation, autoregulation of nodule development, and intracellular accommodation of bacteria, metabolism, and transport supporting SNF to prevent nodule senescence [14].
Salinity stress increases the accumulation of reactive oxygen species (ROS); however, total phenolic content, ascorbic acid content, and antioxidant activity traits were enhanced in 320 tetraploids compared to 84 diploid genotypes of Solanum tuberosum L. [15]. According to the study’s revelations, the concentration of antioxidant compounds correlated positively with the skin tuber color and ploidy levels. In Citrus limon (L.) Osbeck, Bhuvaneswari et al. [16] indicated that cyclic monoterpene, limonene, had significantly increased in tetraploids induced by 0.025% colchicine for 24 h. Limonene is biosynthesized from the precursor geranyl diphosphate (GPP) by enzymatic biotransformation with d-or-l-limonene synthetase. The production of limonene monoterpenes is completed by methyl group deprotonation in the α-terpinyl cation, and this occurs in a wide variety of species, including Conifers, Lamiales, and Pinales, of which some are tetraploids [17][18].
Moreover, overexpression of the terpenoid biosynthesis gene in soybeans influenced the nodulation signaling pathways. The results indicated that the six terpenoid synthesis genes (SoTPS6, SoNEOD, SoLINS, SoSABS, SoGPS, and SoCINS) in soybean hairy roots increased nodule number, nodule root length, and fresh root weight [19]. As reported in other studies, the expression of terpene in the roots was highly coordinated and cell-specific. The abovementioned observations demonstrated the role of ploidy in this largest class of specialized metabolites found within different structures in plants. According to Pott et al. [20], monoterpenes like limonene plays a key role in plant’s interaction with the environment, especially in protecting plants against biotic and abiotic stresses.
Generally, polyploid plants often have improved traits than their diploid relatives and may have a greater advantage in regulating both osmotic and ionic stress. The improved traits or maintained homeostasis plays an important role in many of the functions occurring in polyploidized plant cells. The accepted explanation of the influence of salinity stress is that imbalances in ion content in plant cells affect plant fitness, especially by affecting plant nutritional status and cell water potential, and cause toxic effects through accumulation of ions, which disturb nutrient acquisition and result in cytotoxicity [21][22]. Under stress, polyploidized plants show increased capacity to maintain unequal concentrations of sodium (Na+) and potassium (K+) ions both inside and outside the cells. Such improved responses occur due to tolerance genes and TFs regulating ion Na+/K+ pump and exclusion through selective permeability of plasma membrane proteins (PMP), high sodium affinity transporter (HKT), and Na+/H+ exchangers that help to alleviate ion toxicity in the cells [23][24].
Although information regarding polyploidized leguminous crops’ reaction to toxic ions is very scant, monocotyledous crops such as hexaploidy wheat spp. (Triticum aestivum genome BBAADD) demonstrated improved ion toxicity alleviation than both diploid counterparts and tetraploid wheat progenitors (T. turgidum) or durum wheat (T. durum). In polyploidized rice (HN2026-4x and Nipponbare-4x), Tu et al. [25] reported improved regulation of Na+ content and H+ proton content flux at root tips, with decreased Na+ and increased H+ efflux in the roots. In legumes, the physiological mechanisms explaining the improvement in salt tolerance with increasing levels of ploidy remain under-researched. However, genome duplication has been widely suggested to improve salinity stress resistance through enhanced proton transport pump and homeostasis in various monocot and dicot vegetable crop species [24][25][26].

3. Metabolic Changes of Legume Polyploids Exposed to Salinity Stress

Salinity stress limits crop growth and metabolism, posing major impacts on agricultural productivity. As previously mentioned, over-irrigation systems and drought stress continue to cause oversalinization in many areas used for planting agroeconomically important crops. Salinity stress, also known as hyperionization, poses serious effects on the metabolic and growth processes of plants through excessive accumulation of ions, as previously indicated [27]. Numerous reports have elaborated on NaCl’s effects on growth, mineral composition, proline content, and antioxidant enzyme activity, which dramatically reduces the productivity of many crops.
Additionally, the mean number of seeds per pod and 100-seed weight were increased in all the mutagenic treatments involving gamma rays and EMS in mungbean, urdbean varieties T-9 and Pant U-30 [28]. These mutation-based improvements conferred increased genetic diversity required to achieve economically important traits in both leguminous and non-leguminous crops wherein the selected mutant lines successfully contributed to the diversity of the crop’s genetic base, which is highly required for growth improvement against environmental stresses such as drought and salinity. Furthermore, the genetic variability induced through mutagenesis in treated populations also demonstrated some level of genotype dependency, as reported by Laskar et al. [29] in lentils (Lens culinaris Medik). The genome structure in polyploids also has implications for both physiology and stress responses during vegetative and reproductive growths. As reports showed that polyploidy has occurred at least once in angiosperm lineages, the significantly altered phenotypes often influence the interactions of polyploids towards both biotic and abiotic stress constraints. According to Forrester and Ashman [1], plant-biotic interaction involving legume-rhizobia mutualism serves as an important interaction that regulates the nutrient cycle, in addition to its indirect impact on vegetative (number of trifoliate leaves, leaf size, shoot height, root length, branch number, etc.) and reproductive growth parameters (flower number, fruit pods, seed number, and 100-seed weight).
Although some researchers found that the notion that autopolyploids are larger than their diploid progenitors does not always hold true, such as the comparison of Arabidopsis and Musa plants, wherein obtained variations brought from haploidy to diploidy showed increases in growth parameters but then decreased with the increase in ploidy levels in both species. Such findings were reported by Corneillie et al. [30] in A. thaliana and Brisibe and Ekanem [31] in Musa species. Quantitatively and qualitatively studying these differences in mutant plants can allow scientists to infer the functions of duplicated genes or map certain mutations on the chromosomes. Furthermore, such studies must continue to selectively breed crops to produce varieties that have higher yields or varieties adapted to specific environmental conditions and are resistant to plant pathogens.

4. Gene Expression and Symbiosis in Polyploids Grown under Salinity Conditions

Although a detailed understanding of the molecular and physiological mechanisms explaining the improvement in salinity stress tolerance with increasing levels of ploidy in leguminous crops remains scant. Tossi et al. [32] reported the change in some leaf traits that favored abiotic stress tolerance in Arachis duranensis × A. ipaensis synthetic allotetraploids. In urdbean (Vigna mungo (L.) Hepper), mutagenized genetic variability contributed to improved phenotypic traits in M2 and M3 generations [28]. Chao et al. [33] earlier reported improved salinity stress resistance in autopolyplodized Arabidopsis thaliana through enhanced potassium (K) accumulation in root and mesophyll tissues. The study revealed that ploidy level was a significant determinant of leaf K concentration attributed to the 57.2% variations observed in tetraploids, constituting a 32% K-level increase in these plants compared to the diploid lines. Furthermore, the findings showed that autotetraploid accession Wa-1 (Warsaw, Poland) contributed additional alleles for increased leaf K with no obvious traits found in their diploid counterparts. According to Munns and Tester [34], increased K/Na ratio enhanced tolerance to osmotic and ionic components of salinity stress, as similarly reported by Chao et al. [33].
Isayenkov and Maathuis [35] also reported the adaptation to adverse environmental salinity stress conditions in polyploidized plants driven by genes related to the efficient operation of NADPH-dependent ‘ROS-Ca2+ hub’. This multigenic family of calcium-dependent protein kinase encodes structurally conserved unimolecular calcium sensors or protein kinase effector proteins [36]. As reported in previous studies, Ca2+-dependent protein kinase diversity could be amplified by splicing and post-translational modifications [37], with a proposition that these protein kinases follow a common regulatory mechanism through phosphorylation [38] to confer tolerance to salinity stress. Hexaploidy lines of Ipomoea trifida reportedly exhibited increased K+ retention while excluding Na+, presenting highly reduced sensitivity of plasma membrane K+-permeability channels in both mature and elongation root zones of plants [39]. The abovementioned ion channel activation occurs as a result of ROS-induced protein modification/membrane-dependent NADPH oxidase system, regulated by the expression of respiratory burst oxidase homolog (Rboh) genes [40][41]. The retainment of high K+ levels and exclusion/accumulation of low Na+ concentrations in the cytosol confers salinity stress tolerance in plants [39].
In many legumes, specific redox-dependent signaling pathways involving ROS, reactive nitrogen species (RNS), and reactive sulfur species (RSS) play a key role in acclimation and tolerance to environmental stress. According to Matamoros and Becana [42], ROS-induced modifications in legumes occur through oxidation, S-nitrosylasion, S-glutathionylation or per sulfidation of the cysteine thiol group, oxidation of methionine residue, nitration of tyrosine residue and lysine/arginine residue carbonylation. Molecular analysis of redox-based post-translational modification of proteins revealed functional implications of these alterations on nodulation and whole plant growth and development under adverse conditions. Even though polyploidy is a major genetic driver of ecological and evolutional diversity in plants, its effects on legume interactions remain partially explored on the mutualistic relationship of legumes with microbes. Such studies, like that of Forrester and Ashman [43], reported that Medicago sativa subsp. caerulea autotetraploid plants produced larger nodules with larger nitrogen fixation zones than diploid plants using two strains of rhizobia, Sinorhizobium meiloti and Sinorhizobium medica. Focal microscopy was used to quantify the internal traits of nodule formation in both diploid and neotetraploid M. sativa plants.
There was a strong direct effect on nodulation and nodule traits such as N-fixation zone, nodule area, and bacteroids containing symbiosomes due to increased ploidy level. These nodule features and other polyploidy-induced unique characteristics involving activation of the nodule-specific transcriptome, node genes within mobile plasmids of rhizobial genomes, and ample nodule-specific cysteine-rich (NRC) genes were reported. NCR gene family is extensively large in Medicago spp. with about 600 other genes [44][45]. The wider availability of such genome sequence information of Medicago and several other legume species will boost genomic research and breeding for yield improvement and adaptation of plants to adverse conditions. RNA sequencing transcriptome analyses in polyploids provided information into the transcriptional mechanisms, molecular mediation of various cellular processes, genome reprogramming, and gene function.
Some of the genes, like leginsulin, defensins, root transporters, nodule-related genes, and circadian clock genes, are widely explored across legume species in relation to biological symbiotic nodulation systems [46][47][48]. Currently, sufficient information is available in legumes that are required to elucidate responsible genes and cellular processes involved in plant-microbe symbiosis; however, many genes in the nodulation, plant growth, and response to abiotic stress, such as salt and drought stress still need to be investigated. Furthermore, not all genes are upregulated during symbiosis or the period of stress. Genes such as MtDef4.3 of plant defensin genes in M. truncatula be downregulated under rhizobia-induced nodulation for N-fixation [49]. Most of these expressed genes contribute to the morphology, physiology, and developmental attributes, also providing housekeeping functions necessary to normalize the expression, regulation, and response of plants to environmental instabilities.
The WRKY genes encoding WRKY proteins containing conserved sequence WRKYGQK heptapeptide at the N-terminal end have also been widely implicated in leguminous and non-leguminous crop tolerance to biotic and abiotic stress. Although WRKY evolution in legumes is still unknown, Song et al. [50] reported that this family comprises a class of TFs involved in physiological changes that enhance plant responses under abiotic stress, such as drought and salinity constraints. As alluded to by various other researchers, natural and induced polyploidization via mutagenesis can unleash new alleles of WRKY genes and others that control traits required for salinity stress tolerance.
 

This entry is adapted from the peer-reviewed paper 10.3390/cells12162082

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