Balancing yield trade-off in legumes during multiple stress tolerance via strategic crosstalk by native NAC transcription factors

Abstract

NAC transcription factors are the bonafide regulators of growth and stress-signaling. Disparate signals converge at NACmediated transcriptional programming to initiate a cellular response. Like other stress regulators such as DREB, DDF1, bZIP, PYL, NAC-mediated stress adaptation often compromises beneficial agronomic traits resulting in yield-penalty. Overexpression of these TFs can cause metabolic and hormonal perturbations that exert growth-retardation by activating ABA-hypersensitivity, chloroplast-degradation, or carbon-starvation, resulting in growth arrest and decline in photosynthetic activity. In addition, functional conservation of non-native members is unpredictable due to the non-conserved C-terminal part of the NAC proteins, hence limiting the utilization of well-studied orthologous genes in legumes. The growth/tolerance trade-off is an unresolved mystery. The co-occurrence of multiple stresses further perplexes the broadrange stress improvement of legume crops. To overcome the trade-offs, we need to understand the growth checkpoints that crosstalk with mediated by the stress-responsive gene candidate. Interestingly, NAC proteins appear to be the branch-point of ABA-dependent and ABA independent signaling hence can activate/repress a non-overlapping set of genes associated with stress response and growth to avoid the detrimental crosstalk. Indeed, a versatile NAC member improving both stress adaptation and yield simultaneously through synergistic crosstalk holds the key for sustainable legume improvement. Moreover, the successful manipulation of stress signaling depends on non-interfered ABA signaling of stress responses and growth, as well as strengthening of carbon assimilation. Photosynthesis plays a central role in plant carbohydrate metabolism and stress recovery by restoring the energy status. Hormones and carbohydrates participate together in a complex stress-signal transduction system. For instance, ABA antagonistically regulates growth and sugar signals. Native NAC candidates isolated from robust genetic sources like cowpea can be a useful approach to overcome trade-offs and achieve a desired phenotype. This review provides new insights to improve legume yield via transcriptional reprogramming.

Cowpea NAC1/NAC2 transcription factors improve growth and tolerance to drought and heat in transgenic cowpea through combined activation of photosynthetic and antioxidant mechanisms

“…Our earlier studies demonstrated that overexpression of VuNAC1/2 in Arabidopsis showed improved photosynthesis and recovery from aluminum, cadmium, H 2 O 2 , NaCl, sorbitol, PEG, and NaCl stress under nutrition‐limiting conditions (Srivastava et al, 2022). The observations in the yeast model also advocated the involvement of VuNAC1/2 in the salvage of purines and biosynthesis of ATP to power plant growth (Srivastava and Sahoo, 2021a). The current translational study in the native system provides direct evidence for the involvement of VuNAC1/2 in channeling the photosynthetic assimilation toward the organic reserves and armoring the plants against multiple abiotic stresses.…”

“…For the overexpression study, the 888 bp open reading frame (ORF) sequences isolated in our earlier study (Srivastava and Sahoo, 2021a; Srivastava et al, 2022) that encode VuNAC1 (Accession: OM141592) and VuNAC2 (Accession: OM141593) TFs were cloned in pBEAB the binary vector (Figure S1B), followed by cowpea transformation. For VIGS, the 300 bp non‐conserved gene regions from the 3'‐end (Figure S8A) were cloned at the BamH1 and KpnI restriction sites in the pTRV2 vector (Figures 7A, S8B).…”

“…The expression of these genes was signaled by light, abscisic acid (ABA), and methyl jasmonate (MeJA) under optimum growth conditions and showed stable induction by dehydration, NaCl, aluminum, heat, and cold. The proteins recognize MYC‐like “CATGTCCACG” motif for DNA‐binding, and homo/heterodimerization is necessary for the transactivation activity (Srivastava and Sahoo, 2021a). The present study investigated the morphological and agronomic phenotypes of VuNAC1/2 and their response to multiple yield‐limiting abiotic stresses such as drought, salt, heat, and cold through their constitutive overexpression in a commercial cowpea variety.…”

Low Temperature Stress Tolerance: An Insight Into the Omics Approaches for Legume Crops

“…To date, individual genes had a limited impact on stress tolerance in plants. However, the simultaneous activation of a subset of those genes by transcription factors is a promising technique (Srivastava and Sahoo, 2021). It has been shown that transgenic plants containing AP2/EREBP genes (DREB1A) can enhance abiotic stress tolerance in crop plants (Singh et al, 2012).…”

Isolation, characterization, and functional verification of salt stress response genes of NAC transcription factors in Ipomoea pes-caprae

“…With the development of biotechnology, NAC TFs in different species have been identified, including 117 in Arabidopsis thaliana ( Ooka et al., 2003 ), 151 in Oryza sativa ( Nuruzzaman et al., 2010 ), and 152 in Nicotiana tabacum ( Rushton et al., 2008 ). As one of the largest transcription families in plants, NAC TFs have many functions, such as in plant secondary metabolism ( Srivastava and Sahoo, 2021 ), plant development and senescence ( Gong et al., 2020 ), and hormone regulation ( Tao et al., 2022 ). In response to high salt, drought, and high temperatures, NAC TFs play an important regulatory function by activating or inhibiting the expression of target genes and improving abiotic stress tolerance ( Trishla and Kirti, 2021 ; Guo et al., 2022 ).…”