Phosphate or nitrate imbalance induces stronger molecular responses than combined nutrient deprivation in roots and leaves of chickpea plants

Abstract

The negative effects of phosphate (Pi) and/or nitrate (NO3−) fertilizers on the environment have raised an urgent need to develop crop varieties with higher Pi and/or nitrogen use efficiencies for cultivation in low‐fertility soils. Achieving this goal depends upon research that focuses on the identification of genes involved in plant responses to Pi and/or NO3− starvation. Although plant responses to individual deficiency in either Pi (–Pi/+NO3−) or NO3− (+Pi/–NO3−) have been separately studied, our understanding of plant responses to combined Pi and NO3− deficiency (–Pi/–NO3−) is still very limited. Using RNA‐sequencing approach, transcriptome changes in the roots and leaves of chickpea cultivated under –Pi/+NO3−, +Pi/–NO3− or –Pi/–NO3− conditions were investigated in a comparative manner. –Pi/–NO3− treatment displayed lesser effect on expression changes of genes related to Pi or NO3− transport, signalling networks, lipid remodelling, nitrogen and Pi scavenging/remobilization/recycling, carbon metabolism and hormone metabolism than –Pi/+NO3− or +Pi/–NO3− treatments. Therefore, the plant response to –Pi/–NO3− is not simply an additive result of plant responses to –Pi/+NO3− and +Pi/–NO3− treatments. Our results indicate that nutrient imbalance is a stronger stimulus for molecular reprogramming than an overall deficiency.

Differential metabolic rearrangements in the roots and leaves of Cicer arietinum caused by single or double nitrate and/or phosphate deficiencies

“…One possible interpretation of the decline in glucose‐6‐phosphate in both organs is the rapid isomerization of glucose‐6‐phosphate to fructose‐6‐phosphate, especially in the roots of chickpea plants, through glycolysis in response to Pi deficiency. This finding is supported by our previous suggestion (Nasr Esfahani et al., 2021) that under Pi deficiency, glycolysis continues through the induction of the SS/UDP‐glucose pyrophosphorylase pathway and the glycolytic pathway using phosphoenolpyruvate carboxylase/malate dehydrogenase/NAD‐malic enzyme, and thus bypassing the reaction catalyzed by pyruvate kinase despite low adenylate and Pi concentrations in both organs (Figure 7).…”

“…SK1 and ADT1 ) were downregulated in roots under NO 3 − starvation and/or double nutrient deficiency (Figure 6), whereas the levels of methionine, proline and the aromatic AAs tryptophan, tyrosine and phenylalanine were not declined in the roots by the same nutrient stress treatments (Figures 4 and S8; Table S1). Furthermore, in the roots and leaves of chickpea plants grown under NO 3 − starvation and double nutrient deficiency, increased activities of NAD‐GDH (Figure 5b) in parallel with reduced levels of glutamate (Figures 4 and S8; Table S1) and decreased activities of NADH‐glutamate synthase (GOGAT; Nasr Esfahani et al., 2021) could likely reflect the possibility that N assimilation through NADH‐GOGAT was substituted by deamination of glutamate to NH 4 + and α‐ketoglutarate by NAD‐GDH (Krapp et al., 2011). A similar shift in primary N assimilation in response to changes in N availability has been described in barley ( Hordeum vulgare ; Fataftah et al., 2018).…”

“…Results of this study, however, indicated that while the levels of fructose‐6‐phosphate, glucose, fructose and sucrose remained unchanged in the leaves under Pi deficiency, their levels increased in roots under the same conditions (Figures 4 and S8; Table S1). These findings, as well as a greater activity of sucrose synthase (SS) in the roots than in leaves under low‐Pi conditions (Nasr Esfahani et al., 2021), could reflect enhanced activities of glycolysis and the TCA cycle in the roots, relative to the leaves, of chickpea plants under Pi‐deficient conditions. This is plausible because high activities of glycolysis and TCA cycle in the roots are essential in Pi‐efficient plants under Pi‐deficient conditions to enable the sustained production and secretion of OAs from roots into the rhizosphere (Plaxton & Tran, 2011).…”

“…This is plausible because high activities of glycolysis and TCA cycle in the roots are essential in Pi‐efficient plants under Pi‐deficient conditions to enable the sustained production and secretion of OAs from roots into the rhizosphere (Plaxton & Tran, 2011). Greater activity of SS in the roots than in the leaves of chickpea plants under low‐Pi conditions (Nasr Esfahani et al., 2021) could increase sucrose transport from the shoots to roots, and therefore stimulate Pi‐transporters for improving Pi uptake (Hammond & White, 2008; Lemoine et al., 2013). Therefore, according to these findings, chickpea could be suggested as a Pi‐efficient plant in terms of metabolic adaptation to Pi deficiency.…”

Increased Carbon Partitioning to Secondary Metabolites Under Phosphorus Deficiency in Glycyrrhiza uralensis Fisch. Is Modulated by Plant Growth Stage and Arbuscular Mycorrhizal Symbiosis

“…Previous studies demonstrated that plants increased tissue C partitioning from non-structural carbohydrates (NSCs; e.g., soluble sugar and starch) toward secondary metabolites (SMs), such as flavonoids, under P limitation ( Sampedro et al, 2011 ; Liu et al, 2016 ; Shinde et al, 2018 ; Mo et al, 2019 ). Rather than consuming P, secondary metabolism can recycle P from phosphate esters and produce reducing equivalents to scavenge free radicals that are induced by P deficiency ( Malhotra et al, 2018 ; Nasr Esfahani et al, 2021 ). However, according to the growth-differentiation balance hypothesis (GDBH) ( Herms and Mattson, 1992 ), trade-offs of C allocation and partitioning between growth and secondary metabolism exist.…”