The rice OsNAC6 transcription factor orchestrates multiple molecular mechanisms involving root structural adaptions and nicotianamine biosynthesis for drought tolerance

Abstract

SummaryDrought has a serious impact on agriculture worldwide. A plant's ability to adapt to rhizosphere drought stress requires reprogramming of root growth and development. Although physiological studies have documented the root adaption for tolerance to the drought stress, underlying molecular mechanisms is still incomplete, which is essential for crop engineering. Here, we identified OsNAC6‐mediated root structural adaptations, including increased root number and root diameter, which enhanced drought tolerance. Multiyear drought field tests demonstrated that the grain yield of OsNAC6 root‐specific overexpressing transgenic rice lines was less affected by drought stress than were nontransgenic controls. Genome‐wide analyses of loss‐ and gain‐of‐function mutants revealed that OsNAC6 up‐regulates the expression of direct target genes involved in membrane modification, nicotianamine (NA) biosynthesis, glutathione relocation, 3′‐phophoadenosine 5′‐phosphosulphate accumulation and glycosylation, which represent multiple drought tolerance pathways. Moreover, overexpression of NICOTIANAMINE SYNTHASE genes, direct targets of OsNAC6, promoted the accumulation of the metal chelator NA and, consequently, drought tolerance. Collectively, OsNAC6 orchestrates novel molecular drought tolerance mechanisms and has potential for the biotechnological development of high‐yielding crops under water‐limiting conditions.

Regulatory changes in TaSNAC8‐6A are associated with drought tolerance in wheat seedlings

“…In agreement with this finding, similar effects on yield have also been observed in transgenic rice overexpressing OsNAC5, OsNAC6 and OsNAC9 (Jeong et al, 2013;Lee et al, 2017;Redillas et al, 2012). However, when OsNAC5, OsNAC6 and OsNAC9 were overexpressed in rice driven by a root-specific (RCc3) promoter, the grain yields were significantly increased under both well-watered and water-limited conditions (Jeong et al, 2013;Lee et al, 2017;Redillas et al, 2012). Future investigation would incorporate tissue-specific promoters, such as RCc3, for optimization of TaSNAC8-6A overexpression for wheat production under field conditions.…”

“…Importantly, under well‐watered conditions, both transgenic lines exhibited more extensive root systems than WT (Figure S8b), which could plausibly contribute to the observed yield gain. In agreement with this finding, similar effects on yield have also been observed in transgenic rice overexpressing OsNAC5 , OsNAC6 and OsNAC9 (Jeong et al , ; Lee et al , ; Redillas et al , ). However, when OsNAC5 , OsNAC6 and OsNAC9 were overexpressed in rice driven by a root‐specific (RCc3) promoter, the grain yields were significantly increased under both well‐watered and water‐limited conditions (Jeong et al , ; Lee et al , ; Redillas et al , ).…”

“…However, little is yet known about which genes in the auxin signalling pathway may be directly targeted by NAC transcription factors. TaSNAC8-6A overexpression in both Arabidopsis and wheat enhanced their drought tolerance and improved root system development ( Figure 5; Figure 6), which was also observed in transgenic Arabidopsis overexpressing AtNAC2 (He et al, 2005) and transgenic rice overexpressing OsNAC6 (Lee et al, 2017).…”

“…The NAC (NAM, ATAF1/2 and CUC2) proteins comprise a large family of plant-specific TFs whose members participate in a range of regulatory and developmental processes, including growth and differentiation at the shoot apical meristem (Takada et al, 2001), root development (Xie et al, 2000), leaf senescence (Yang et al, 2011), formation of secondary cell walls (Mitsuda et al, 2007), nutrient remobilization to grains (Uauy et al, 2006) and abiotic stress response (Nakashima et al, 2012;Shao et al, 2015). Many stress-responsive NAC proteins fall into one group (Nakashima et al, 2012;Nuruzzaman et al, 2010), such as ATAF1, ANAC019, ANAC055, ANAC072, AtNAC2 and AtNAP from Arabidopsis (He et al, 2005;Sakuraba et al, 2015;Tran et al, 2004;Wu et al, 2009); SNAC1, OsNAC5, OsNAC6, OsNAC10 and OsNAP from rice (Chen et al, 2014;Hu et al, 2006;Jeong et al, 2010;Jeong et al, 2013;Lee et al, 2017); and ZmSNAC1, ZmNAC55 and ZmNAC111 from maize (Lu et al, 2012;Mao et al, 2015;Mao et al, 2016).…”

<strong>When water runs dry and temperature heats up: </strong><strong>Understanding the mechanisms in rice tolerance to drought and </strong><strong>high temperature stress conditions</strong>

“…For example, overexpression of OsNAC6, OsNAC10, OsNAC9 and OsNAC5 in rice improved drought tolerance through increased root number and diameter (Lee et al, 2016a). Tolerance conferred by overexpression analysis was suggested to be mediated either by nicotianamine (NA) biosynthesis, glutathione relocation, or by incorporating and controlling factors involved in cell wall biosynthesis (Lee et al, 2016a, Lee et al, 2016b, Jeong et al, 2010, Redillas et al, 2012, Jeong et al, 2013. Transgenic rice plants overexpressing SNAC1 showed drought resistance both at the vegetative and reproductive stage by reducing water loss through regulation of stomatal opening possibly by regulating the expression of OsSRO1c but with no compromise in photosynthesis , Hu et al, 2006.…”