miRNA mediated regulation of NAC transcription factors in plant development and environment stress response

Plant Gene xxx (xxxx) xxx–xxx

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Plant Gene journal homepage: www.elsevier.com/locate/plantgene

miRNA mediated regulation of NAC transcription factors in plant development and environment stress response Yuniet Hernández, Neeti Sanan-Mishra⁎ Plant RNAi Biology Group, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India

A R T I C L E I N F O

A B S T R A C T

Keywords: MiRNA NAC transcription factors Structural features Evolution Duplication Functionalization

NAC genes comprise one of the largest families of plant transcription regulators that are known to play crucial roles in various developmental processes and stress responses. Evolutionary expansion of the gene family in land plants probably added to the functional diversity of the gene family. The ongoing research has analyzed the differential expression patterns of the NAC transcription factors under various stresses for determining their plausible role during adaptive stress response in plants. However, the complex molecular mechanism regulating NAC gene expression and function is still elusive. The discovery of miRNAs, as a novel class of regulatory factors, has shed new light on the regulatory mechanisms that define the functional domains of the transcription factors. In this context studies on miRNA-mediated regulation of NAC gene expression in plant development have provided critical evidence for multi-layered control of the transcription factors. The review describes the divergent role of NAC transcription factors, which were initially thought to be only involved in vasculature development in plants. The structural features of the NAC transcription factors and the evolution of the gene family have also been discussed. Special focus is placed on the regulation of NAC-TFs by miRNAs to understand the developmental networks operating in the plants in response to abiotic stress and hormone cues.

1. Introduction The recent trends of climate change are increasingly threatening agricultural productivity and global food security. Hence, supplying enough food for the constantly increasing world population under changing weather conditions is a major challenge faced by agricultural biotechnologists. Improving plant tolerance to abiotic stresses is an important strategy for mitigating the consequence of climate change (Abdallah et al., 2014). The effectiveness of scientific methodologies will be ensured when the genetic basis of stress tolerance is better known and the responses to abiotic stress are understood. In the sessile plant world growth and organ development is a continuous process that is regulated in response to the environmental cues. The genetic circuits incorporate numerous regulatory networks that may operate in an organ or tissue preferential manner. At the cellular level this involves coordinated action of several genes in response to the signaling cascades. The differential gene expression is regulated at the level of transcription and post-transcription by the transcription factors (TFs) and microRNAs (miRNAs), respectively. The TFs bind to promoters of miRNA genes to regulate spatio-temporal expression of primary miRNA transcripts (Johnson et al., 2003; Martinez et al., 2008), likewise the differential expression of TFs is in part regulated by the

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miRNAs. Both players comprise of diverse members encoded by large gene families and have a widespread impact on gene expression. Over the last few decades extensive literature has accumulated on the importance of the combinatorial regulation of TFs and miRNAs for the appropriate modulation of biological processes (Hobert, 2004; Cui et al., 2007; Arora et al., 2013). The NAC proteins constitute one of the largest families of plantspecific TFs that is present in a wide range of plants (Wang et al., 2011). They are known to play an important role in plant development and stress responses, including wounding, bacterial or viral infection (Collinge and Boller, 2001; Hegedus et al., 2003). The name NAC derives from the founder members, which include Petunia NAM (no apical meristem), Arabidopsis ATAF (Arabidopsis transcription activation factor) and Arabidopsis CUC (cup shaped cotyledon) genes. The cDNA encoding a NAC protein was first reported from Arabidopsis as RD26 (responsive to dehydration 26) gene (Yamaguchi-Shinozaki et al., 1992; Aida et al., 1997). The transcription activation property of NAC proteins were identified when Arabidopsis ATAF1/2 and AtNAM (NARS2) proteins were found to activate the CaMV-35S promoter in yeast cells. This was followed by the identification of three Arabidopsis NAC proteins (ANAC019, ANAC055 and ANAC072/RD26) and their functional analysis in response to drought stress. Since then literature is replete with

Corresponding author. E-mail address: [email protected] (N. Sanan-Mishra).

http://dx.doi.org/10.1016/j.plgene.2017.05.013 Received 9 January 2017; Received in revised form 8 May 2017; Accepted 23 May 2017 2352-4073/ © 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Hernandez, Y., Plant Gene (2017), http://dx.doi.org/10.1016/j.plgene.2017.05.013

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and D subdomains. However, recently it has been reported that some StNAC and BdNAC proteins do not share this conserved feature (Singh et al., 2013; You et al., 2015) and instead contain completely different sequences resembling a TM motif. Such membrane-associated NAC-TFs are called NTL (NAC with Transmembrane motif 1 Like) (Fang et al., 2008). A typical NTL protein has one or two strong α-helical TM motifs at their C terminus, which directs its association with the plasma membrane or endoplasmic reticulum (Puranik et al., 2012; Yang et al., 2014; Li et al., 2016). Other variants of NAC proteins may contain only the NAC domain or NAC domains repeated in tandem (Singh et al., 2013). Additionally a tyrosine kinase domain was found in one member of StNAC family. Although, additional experimental evidence is required to define the role of the tyrosine kinase domain, it is predicted to regulate the NAC domain activity by autophosphorylation (Singh et al., 2013). In the same way, a plant defense response AAA-ATPase domain/NB-ARC domain was identified in a SiNAC (Setaria italica NAC) indicating a putative involvement of this protein in biotic stress response (Puranik et al., 2013).

the identification of NAC-TFs from different plant species and their association with diverse pathways related to plant stress responses (de Oliveira et al., 2011; Nuruzzaman et al., 2013; Hussey et al., 2015; Pascual et al., 2015; Li et al., 2016; Lv et al., 2016; Wu et al., 2016; Shen et al., 2017). Recent reports have described members of the NACTF family as potential targets of miRNA mediated silencing (Rhoades et al., 2002; Guo et al., 2005; Matts et al., 2010). Hence, it is of utmost importance to understand the intricate regulation of plant stress responses so that an effective strategy for improving the stress tolerance can be designed. In this review, we have summarized the structural features of the NAC-TFs, evolution of the gene family and the various roles of NACTFs. The regulation of NAC-TFs by miRNAs is discussed to understand the developmental networks operating in the plants in response to abiotic stress and hormone cues. 2. Structure feature of NAC transcription factors The members of the NAC-TF family contain a conserved N-terminal DNA-binding NAC domain and a highly variable C-terminal domain that plays a major role in the regulation of transcription (Tran et al., 2004; Olsen et al., 2005). The NAC domain is responsible for nuclear localization, DNA binding and dimerization. The N-terminus NAC domain is approximately 150 amino acids in length and contains five conserved regions (A to E). The subdomain A has the potential to form a helical structure and may be involved in the formation of functional dimers. Both homodimers and heterodimers of the NAC proteins have been reported (Olsen et al., 2005; Jensen et al., 2010; Singh et al., 2013). The nuclear localization signal is located within the subdomain D and the DNA binding activity is associated with subdomain C. This suggests that subdomains C and D are essentials for the functionality of NAC proteins. The subdomains B and E may be responsible for the functional diversity of NAC genes (Kikuchi et al., 2000; Ernst et al., 2004; Jensen et al., 2010). The functional dimers formed by the NAC domains were identified in the X-ray crystallography studies on the Arabidopsis protein, ANAC019 (Arabidopsis thaliana NAC019). The structure revealed that the NAC domain consists of two, asymmetric short ά helix monomers surrounding a twisted beta-sheet. Both monomers differ in the Nterminal tail region, which probably has a role in determining the conformation of each monomer (Ernst et al., 2004). The NAC domain of ANAC019, shares structural similarity with SNAC1 (Stress responsive NAC1 Oryza sativa), StNAC (Solanum tuberosum NAC) and BdNAC (Brachypodium distachyon NAC) proteins (Jensen et al., 2010; Chen et al., 2011; Singh et al., 2013; You et al., 2015). In contrast to NAC domain, the transcription regulatory domain (TRD) at the C-terminal region is highly divergent. Nevertheless some conserved motifs have been identified within this domain in specific NAC-TFs (Hussey et al., 2015; Pascual et al., 2015; Lv et al., 2016). It was reported that conserved motifs have common features including predominance of polar residues and few highly conserved hydrophobic residues (Dyson and Wright, 2005; Jensen et al., 2010). It was speculated that the specific and specialized function of the NAC proteins might be due to the specific amino acid motifs conserved among the members of a NAC sub-family. In silico analysis of the NAC protein Ctermini performed by Jensen et al. (2010) showed that they have a large degree of intrinsic disorder, which could be useful for systematic analysis of structural ID. In addition, the C-terminal domains of some NAC proteins are involved in protein binding and the others may contain trans-membrane (TM) motifs (Nuruzzaman et al., 2010; Pascual et al., 2015; Zhu et al., 2015). Various NAC sub-families in diverse species contain 2–5 subdomains (Singh et al., 2013; Pascual et al., 2015; Zhu et al., 2015; Lv et al., 2016) among which subdomains C and/or D are found to be present in most cases. A typical N-terminal NAC domain contains highly conserved A, C

3. Origin and evolution of genes encoding the NAC-TFs The identification of NAC proteins in the moss Physcomitrella patens and most vascular plants together with their absence in some green algae led to the presumption that they are exclusively present in land plants (Maugarny-Calès et al., 2016). This also indicated that the expansion of the NAC family occurred after the divergence of tracheophytes or vascular plants (Xu et al., 2014). However, the myth was busted by the recent discovery of functional NAC-TF in members of green algae. According to Maugarny-Calès et al. (2016), NAC-TF gene family may have appeared around the divergence of the Klebsormidiale algae from other streptophytes. It was observed that VNS-NAC proteins including the VASCULARRELATED NAC-DOMAIN (VND), NAC SECONDARY WALL THICKENING PROMOTING FACTOR (NST) and SECONDARY WALLASSOCIATED NAC DOMAIN PROTEIN1 (SND1); belonging to different sub-families were associated with xylem and fiber cells in both plant groups. This suggested that the NAC proteins might have contributed to the evolution of both water-conducting and supporting cells during the adaptation of plants to land (Xu et al., 2014). However, the identification of Arabidopsis homologues of Zygnematophyceae NAC genes associated to SOG1 (SUPPRESSOR OF GAMMA RESPONSE 1), SND2 and SND3, suggested their involvement in adaptation to DNA-damaging factors and/or in the production of specific cell-wall modifications. Therefore, it was hypothesized that NAC-TFs may have facilitated the initial plant colonization to land and their adaptation to environmental conditions. It is most likely that subsequent to their divergence from other streptophytes and after the establishment of plants to land, the first expansion of the NAC family occurred. The second occurred in flowering plants after their divergence from other vascular plants (Maugarny-Calès et al., 2016). Gene duplication is increasingly recognized as the chief mechanism that contributed to evolution and high diversification of NAC family genes (Ren et al., 2014; Voordeckers et al., 2015). Ancient polyploidy or whole genome duplication (WGD) events might have directly influenced the increase in number of plant NACs and their complexity (Voordeckers et al., 2012). The evolution of NAC-TF gene family may have favored, at least in part, the origin and fast diversification of angiosperm lineages (Magadum et al., 2013). 3.1. Duplication of NAC genes A duplicated gene provides a greater, less-constrained chance for natural selection to shape a novel function (Long et al., 2003). Most of the flowering plants have undergone one or more ancient WGD followed by other gene duplication events like tandem duplication, 2

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Ascertainable hypothesis suggests that the sub-functionalized gene copies undergo purifying selection, whereas the neofunctionalized gene copies are expected to undergo positive selection or relaxed purifying (Li et al., 2016). According to Raes and Van (2003), positive selection is rare, episodic and difficult to detect. To date, evidence of positive selection on duplicated NAC genes has only been referred for the PNAC141/143 and GmNTL6/15 genes from Populus and Glycine max respectively, where expression pattern supports divergence of function by neofunctionalization (Hu et al., 2010; Li et al., 2016). Most of the NAC genes appear to have evolved under purifying selection (Puranik et al., 2013; Hussey et al., 2015; Li et al., 2016). Therefore, for these gene families, sub-functionalization may be a temporary state that facilitates the acquisition of novel functions (Rastogi and Liberles, 2005). Protein subcellular re-localization might be another mechanism for the functional divergence and emergence of new function of duplicated NAC-TF genes. Although the NAC-TFs are usually located in the nucleus, some of them can be found associated with the membranes, while a few might be present in different organelles or the cytoplasm. Based on the subcellular localization predictions in Citrullus lanatus (water melon), some duplicated NAC genes were located in chloroplasts, mitochondria and cytoplasm (Lv et al., 2016). Even though these predictions must be validated, the putative subcellular localizations of ClNAC might indicate functional diversification among these duplications, as proteins could alter their function when relocalized to a new subcellular structure (Ren et al., 2014). Hence the possible changes in cellular roles, or functional diversification of the duplicated ClNAC gene products in new cellular locations should be studied in order to know if they imply some adaptive significance for water melon and consequently for the expansion of ClNAC gene family.

proximal duplication and so on, each of which may make different contributions to evolution (Freeling, 2009). The expansion of NAC-TF gene family appears to have arisen from multiple gene duplication events such as tandem, segmental, proximal, dispersed and/or DNA based transposed duplication (Singh et al., 2013; Wang et al., 2013). In Eucalyptus grandis, the proportion of NAC genes distributed in tandem array surpassed 60%, suggesting that tandem gene duplication have been essential to divergence among EgrNAC gene family members and therefore, to its adaptation to the often harsh Australian climate (Hussey et al., 2015). Conversely, StNAC and VvNAC (Vitis vinifera NAC) gene families have primarily expanded through segmental duplication rather than by tandem repetition (Singh et al., 2013; Wang et al., 2013). So depending on the species, both tandem and segmental duplication might have played a key role in the expansion of this gene family (Nuruzzaman et al., 2010; Puranik et al., 2013; Singh et al., 2013; Wang et al., 2013; You et al., 2015). In recent years, studies of synteny and gene collinearity have become increasingly important for tracing the evolutionary histories of both genomes and gene families (Wang et al., 2012; Xu et al., 2016). Interestingly, duplicated NAC gene can be found at syntenic/collinear position on angiosperm chromosomes (Hu et al., 2010; Shang et al., 2013; Wang et al., 2013; Li et al., 2016; Shang et al., 2016). Analysis of Populus NAC gene-duplicated clusters revealed that 87 out of 120 NAC genes were preferentially retained duplicated blocks associated with the recent segmental duplication events (Hu et al., 2010). It was suggested that the same evolutionary force might have contributed to the evolution of 19 paralogous pairs localized in conserved positions on segmental duplicated blocks. The tandem duplication analysis of six pairs of NACs revealed that the occurrence of local duplications was prior to the chromosomal segment duplication. Thus, different modes of gene duplication may have directed the multifarious evolutionary patterns of the NAC gene family.

4. miRNA biogenesis and function The NAC-TFs function as important components in complex signaling progress during plant development (Kim et al., 2016; Shang et al., 2016) and stress responses (Gao et al., 2016). Similar to other cellular transcripts involved in cell-fate determination, the NAC transcripts are predominant targets of post-translational gene silencing (PTGS) mechanism (Rhoades et al., 2002). The 21 to 24 nt long miRNAs are among the most abundant and well characterized class of small RNA species that regulate various aspects of plant growth and development (He et al., 2013; Lastdrager et al., 2014; Ripoll et al., 2015). miRNAs are involved in almost all physiological processes such as primordial development, organ formation, apical dominance, shoot branching, panicle formation, lateral root development etc. by regulating the expression of key genes and transcription factors (Kebrom et al., 2013; Fan et al., 2015; Xie et al., 2015). Some miRNAs are also known to be involved in hormonal biosynthesis and signaling such as gibberellins and auxins (Mallory et al., 2004; Xia et al., 2012; Liu et al., 2016). Some of them help in maintaining genome integrity by silencing transposable elements (Zlotorynski, 2014). miRNAs are also known to be the regulators of different biotic as well as abiotic stresses in plants. The biogenesis of plant miRNAs is an intricate process including several proteins complexes. In plants the miRNA genes are transcribed by DNA dependent RNA polymerase II inside nucleus, to form primiRNA (primary miRNA) transcripts (Kurihara and Watanabe, 2004; Xie et al., 2005; Kim et al., 2011) which are then processed into a stem loop structured pre-miRNA (precursor miRNA) in the dicing bodies (D bodies) or small nuclear RNA binding protein D3 bodies (SmD3-bodies) by DICER-LIKE 1 (DCL1) activity (Han et al., 2004; Kurihara and Watanabe, 2004; Fang and Spector, 2007; Fujioka et al., 2007). The major proteins involved in miRNA processing that were detected by bimolecular fluorescence complementation (BiFC) include HYPONASTIC LEAVES 1 (HYL1), a nuclear dsRNA binding phosphoprotein (Han et al., 2004; Vazquez et al., 2004), SERRATE (SE), a C2H2-zinc finger protein (Ori et al., 2000; Yang et al., 2006), TOUGH (TGH), an RNA binding protein with a G-patch and a SWAP domain (Ren et al.,

3.2. Functionalization of the duplicated NAC genes The diversification of gene function after duplication has been given substantial attention in genome-wide studies (Galimba and Di Stilio, 2015; Hu et al., 2015; Zhu et al., 2015; Shang et al., 2016). Duplicated multifunctional genes can have several possible fates. For example, some duplicated genes lose their function over the course of evolution whereas others take on some of the roles of their parental transcription factor, lessening the burden on each copy and giving each copy more flexibility to change. This partitioning of original function is known as sub-functionalization (Force et al., 1999), whereas the acquisition of novel adaptive functions is known as neofunctionalization (Hughes, 1994). TFs generated by gene duplication events are maintained in the genome for a period of time during which they differentiate in some aspects of their function (Magadum et al., 2013). Finally, if one of the duplicates retains the ancestral function while its paralog gains a novel function that contributes to better fitness, selection will act to retain both duplicates. It has been suggested that functional divergence between duplicated genes can affect the gene expression pattern and/or the protein biochemical properties (Li et al., 2016). In Populos, it appears that the homologous pairs PNAC008/010 diverged from each other through sub-functionalization after being generated by segmental duplication, which allowed both to be preserved (Hu et al., 2010). PNAC008 gene was mainly expressed in young leaves and male catkins, whereas its duplicate counterpart PNAC010 gene extended to a broader expression patterns in young and mature leaves, female and male catkins. Similarly, divergence in expression of four duplicated paralogous pairs indicated that Gossypium raimondii NAC genes have also been preserved by stable sub-functionalization (Shang et al., 2013). In this way, generation of paralogs results in modularity within the TF family, because each paralog endows the others with greater freedom to change (Cheatle Jarvela and Hinman, 2015). 3

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regulatory functions (Baker et al., 2005) due to the varying spatiotemporal expression patterns of the miRNAs and the targeted NAC genes (Pei et al., 2013; Fang et al., 2014; Wang et al., 2016). An interesting example is provided by Agrostis stolonifera miR319a, with a potential role in the abiotic stress response by indirectly regulating the stress-responsive gene AsNAC60 expression, which is not its natural target (Zhou et al., 2013). A list of miRNAs targeting NAC-TFs and their putative regulatory functions are summarized in Table 1.

2012; Ren and Yu, 2012), Cap binding complex (CBC), a heterodimeric nuclear cap-binding riboprotein (Raczynska et al., 2010), C-TERMINAL DOMAIN PHOSPHATASE-LIKE 1 (CPL1) protein (Lu and Fedoroff, 2000; Hugouvieux et al., 2001; Bezerra et al., 2004; Zhang et al., 2008) and HUA ENHANCER1 (HEN1), a methylase (Li et al., 2005; Yu et al., 2005). It is hypothesized that CPL1 is recruited by SE to the DCL1 complex and regulates the functioning of HYL1 through dephosphorylation. The pre-miRNAs thus generated are further processed by DCL1 into miRNA/miRNA* duplexes. These duplexes are methylated by HEN1 on the 3′ ribose of the last nucleotide of each strand. This methylation prevents the duplexes from degradation (Li et al., 2005; Yu et al., 2005; Li et al., 2016). The mature miRNA duplexes are then transported from the nucleus to the cytoplasm by HASTY (HST) with help of other unknown factors (Park et al., 2005). The guide strand of this duplex is then incorporated into an RNA-induced silencing complex (RISC) complex, which contains AGO1 protein as the core molecule to regulate target gene expression (Baumberger and Baulcombe, 2005; Qi et al., 2005). The guide miRNA strand recognizes the target transcripts by sequence complementarity and marks them for cleavage or translation repression (Carrington and Ambros, 2003; Eldem et al., 2012).

5.1. Role of miRNA targeted NAC-TFs in development The NAC-TFs function as important components in complex regulatory networks operative during plant development (Gao et al., 2016). Plant miRNAs serve as key players in these overlapping genetic networks by regulating the expression of the NAC proteins and other TFs (Eldem et al., 2013). Thus a particular miRNA may control several aspects of a plant developmental program. Most of the NAC genes involved in developmental timing, patterning or cell differentiation are targeted by the conserved miR164 family (Table 1). The At-miR164 targets the transcripts of NAC-TFs that are mainly involved in the regulation of organ architecture and the development of lateral roots (Fang et al., 2014). This includes the five well known genes encoding NAC-TFs cuc1/At3g15170, cuc2/ At5g53950, nac1/At1g56010, At5g07680 and At5g61430. The multifunctional CUC1 and CUC2 have been shown to be involved in shoot apical meristem formation, cotyledon separation during embryogenesis as well as in embryonic and floral development (Aida et al., 1997; Takada et al., 2001; Olsen et al., 2005). In Phyllostachys edulis miR164a might play significant roles in flowering by regulating cuc1 and cuc2. It was observed that transgenic Arabidopsis plants overexpressing pemiR164a showed delayed flowering time (Ge et al., 2016). Recently, it was demonstrated that transgenic 2x35S:miR164a/b lines contained a reduced number of ovules, indicating the role for cuc1 and cuc2 genes in promoting ovule initiation in Arabidopsis and Cardamine gynoecium (Gonçalves et al., 2015). The biological role of individual miRNA family members may also be determined by analysis of loss-of-function mutants in plants (Guo

5. Regulation of NAC-TF by miRNAs The NAC-TFs are important potential targets of the regulatory small RNA mediated post-transcriptional silencing machinery (Fig. 1). Arabidopsis miR164 was the first miRNA predicted to target a subset of genes from the NAC-domain TF gene family (Rhoades et al., 2002; Guo et al., 2005). Since then, the research on miR164 regulated NAC-TFs has progressed substantially for different plant species, with emphasis on development-associated and mechanical stress regulated NAC genes. It was observed that the miR164 targeted NAC domains TF module is conserved across species even though the number of family members varies. For example in soybean, 11 members of miR164 family, each encoded by different gene loci target the NAC-TFs whereas, in Arabidopsis only three members of miR164 are involved (Fang et al., 2014). Although, closely related miRNA family members are predicted to target the same set of NAC transcripts, there can be differences in the

Fig. 1. Schematic representation to show the convergence of stress and hormonal signals on the NAC-TFs to regulate gene expression, including that of the host miRNA transcripts. The miRNAs negatively regulate the NAC transcripts to modulate plant development and stress response.

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Table 1 List of miRNAs targeting NAC-TFs and their putative biological functions. miRNA family

Species

NAC target

Function

Reference

miR164

Populus trichocarpa

NAC-domain protein

Mechanical stress

Arabidopsis thaliana

CUC1 and CUC2; NAC1; NAC2; NAC4

Phyllostachys edulis Switchgrass Solanum lycopersicum

CUC1 and CUC2 NAC-domain protein NAC1

Root development, floral development, cotyledon separation, senescence, ovule initiation, pathogeninduced cell death. Delayed flowering Host defense to ToLCNDV, B. cinerea, P. infestans

Zea mays Oryza sativa Phyllostachys edulis Citrus sinensis Citrus sinensis Populus trichocarpa Agrostis tolonifera Populus trichocarpa Phaseolus vulgaris and Medicago truncatula Citrus sinensis Lycium barbarum

NAC1 NAC-domain NAC1 NAC-domain NAC-domain NAC-domain AsNAC60 NAC-domain NAC-domain

Lateral root number Drought stress Salinity and drought stresses Boron stress Boron stress Cross-talk between biotic and abiotic stress Salt and drought stress Mechanical stress Drought stress

(Lu et al., 2005; Wilkins et al., 2009; Cohen et al., 2010; Li et al., 2011) (Mallory et al., 2004; Baker et al., 2005; Guo et al., 2005; Kim et al., 2009; Gonçalves et al., 2015; Lee et al., 2017) (Ge et al., 2016) (Matts et al., 2010) (Naqvi et al., 2010; Jin and Wu, 2015; Luan et al., 2015) (Li et al., 2012) (Fang et al., 2014) (Wang et al., 2016) (Lu et al., 2015) (Lu et al., 2015) (Zhao et al., 2012) (Zhou et al., 2013) (Lu et al., 2005) (Sosa-Valencia et al., 2016 and 2017)

Boron stress Fruit ripening and pigmentation

(Lu et al., 2015) (Zeng et al., 2015)

miR159 miR166 miR319 miR477 miR1514 miR3946 miR6164

protein protein protein protein protein protein

NAC-domain protein NAC-domain protein

2010; Xie et al., 2015) or nutrient deficiency (Lu et al., 2015). Many of the drought responsive miRNAs modulate root development by targeting the root NAC-TFs (Zhang, 2015). It is generally accepted that a more robust root system with increased root length or root biomass has been considered a positive feature under drought conditions. It was observed that miR319a overexpression improves salt and drought stress tolerance in transgenic plants by significantly downregulating its target genes, including AsNAC60 (Zhou et al., 2013). In rice, most of the up-regulated genes in the miR164-targeted NAC (OMTN) overexpressing plants were down regulated by drought stress, suggesting that the conserved miR164-targeted NAC genes may be negative regulators of drought tolerance (Fang et al., 2014). In a recent study, a stress-related NAC1 from Phyllostachys edulis was characterized. Its ectopic expression in Arabidopsis indicated that PeSNAC1 together with ped-miR164b participated in tolerance to salinity and drought stresses through regulation of root development (Wang et al., 2016). Taken together, these results demonstrate that miRNAs act as critical regulators of gene expression for maintaining normal growth and development in adaptation to abiotic stresses. There are reports that salt and drought responsive miRNA are also involved in adaptive response mechanisms to boron (B) deficiency (Lu et al., 2015). For example, miR159 was down regulated in salt stressed sugarcane leaves (Patade and Suprasanna, 2010) and in B-deficient Citrus sinensis leaves (Lu et al., 2015). B deficiency in plants is caused by drought stress. Significant effect of drought stress on reduction of leaf osmotic potential was observed in B-deficient plants (Hajiboland and Farhanghi, 2011). Identification of miRNA that participate in regulating the combined effect of drought and B-deficit stress might improve the plant tolerance to both environmental stresses. An interesting study performed by Sosa-Valencia et al. (2016) revealed that miR1514a modulates a NAC-TF transcript to trigger phasiRNA formation in response to drought in Phaseolus vulgaris. In water deficit conditions, miR1514a is induced and targets NAC-700 transcript for cleavage and produce phasiRNAs, among which phasiRNA1 is again recruited into AGO1 complexes for PTGS. Similarly in Glycine max, miR1514a targets a NTL9 transcript and triggers the production of phasiRNAs (Arikit et al., 2014). NTL9 has been shown to be an important mediator of osmotic stress responses that affect leaf senescence in Arabidopsis (Yoon et al., 2008). Thus, the study of miRNA targeted NAC-TFs under the environmental stresses will shed a light on the genetic measures adapted to respond/adapt to the stresses.

et al., 2005). The functional analysis of early extra petals 1 (Eep1), a lossof-function allele of miR164c, suggested that the miRNA regulates the number of lower petals in a non-redundant manner by regulating the transcript accumulation of cuc1 and cuc2 (Baker et al., 2005). In the same way, miR164 function in aging-induced cell death and senescence was determined through generation of miR164abc triple mutants in Arabidopsis (Kim et al., 2009). In addition to CUC1 and CUC2, NAC1 plays an important role in lateral root emergence and development (Mallory et al., 2004; Guo et al., 2005; Li et al., 2012). Studies in Zea mays revealed that miR164b/ ZmNAC1 regulates lateral root number differentially in the maize inbred lines 87-1 and Zong3. The miR164b promoter analysis showed higher activity in inbred 87-1 maize than in Zong3 maize, leading to higher expression of mature miR164, which down-regulated ZmNAC1 expression. Thus, this leads to the line 87-1 having fewer lateral root numbers than Zong3 (Li et al., 2012). These results confirmed that miR164 is an important negative regulator of NAC1and differential expression of the miRNA may attribute to the varietal differences observed in wild-type plants of a species (Mallory et al., 2004; Guo et al., 2005). Many of the identified miRNAs that respond to different environmental stresses, also modulate root development by targeting root development related genes and TFs such as ARFs, HD-ZIPs and NACs (Zhang, 2015). miR6164a is another miRNA which may have potential roles in development associated to NAC genes. This miRNA was identified in Lycium barbarum fruits and has been predicted to target LbNAC-TF, a homolog of the tomato NAC4 gene (Zeng et al., 2015). RNAi induced reduced expression of SlNAC4 resulted in delayed fruit ripening and substantially reduced carotenoid content in tomato. This suggested that SlNAC4 is a positive regulator of both ripening and carotenoid accumulation (Zhu et al., 2014). It also indicated that miR6164a might be a novel miRNA involved in Lycium barbarum fruit ripening and pigmentation (Zheng et al., 2009).

5.2. Role of miRNA targeted NAC-TFs in response to abiotic stress Plants utilize several mechanisms for regulating and reprogramming gene expression during abiotic stress response. The miRNA regulatory pathways play a crucial role in controlling the expression of a variety of different stress-regulated genes. In the last five years, a number of studies have examined the role of miR159, miR164 and miR3946 in regulating the NAC-TFs during abiotic stress (Patade and Suprasanna, 5

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homologues in Candida albicans do not regulate the lysine pathway (Pérez et al., 2014). Thus, individual studies to monitor the effect of cisgenic overexpression of NAC factors to stress tolerance need to be carried out in crop plants of interest. Interestingly, although the role of NAC-TFs in response to stress has been well known and many of these molecules have been identified as target of miRNA, to date there is no studies reporting crop improvement to environmental conditions by miRNA technology via NAC regulation. Thus the knowledge of the regulatory action of miRNAs assumes importance as it will lead to the identification of the genetic circuits and signaling cascades associated with the various NAC-TFs. Recently, miRNA technology has emerged as an attractive alternative for engineering tolerance to environmental stresses by manipulation of both desirable and undesirable genes. The main advantage of this new strategy is that the transgene expresses only non-encoding RNAs, so that oral toxicity and digestibility studies are not required (Kamthan et al., 2015). Some recent studies have demonstrated that overexpression of miRNA can improve stress tolerance in transgenic plants (Zhang et al., 2011; Zhou et al., 2013; Shriram et al., 2016). The contrasting effects were observed with over-expression of miR408 in Arabidopsis as it improved plant tolerance to salinity, cold and oxidative stress, but increased sensitivity to drought and osmotic stress (Ma et al., 2015). Conversely, overexpression of miR408 in Cicer arietinum increased drought tolerance. These results indicate that miR408 responds to drought stress in a genotype-dependent manner (Hajyzadeh et al., 2015). Therefore, the miRNA strategy designed for one plant species may not be equally useful for another species (Kamthan et al., 2015). To understand the coordinated effects of the NAC-TFs and miRNAs, it is essential to comprehend the networks in which these regulatory molecules operate. In the coming years, understanding the molecular mechanisms of individual NAC proteins and their intricate regulation by the corresponding miRNA will be an important task. This knowledge will have valuable applications in designing crop plants resilient to the challenges posed by the changing climate conditions.

5.3. Role of miRNA targeted NAC-TFs in plant hormone signaling control Phytohormones are signal molecules produced within the plant that control its growth and development through the regulation of gene expression. Interaction between different phytohormone pathways is essential in coordinating tissue growth in response to environmental changes (Curaba et al., 2014). This process entails the participation of many miRNAs for regulating the overlapping genetic networks associated with plant development and hormone signaling. An excellent example is the operation of miR164-mediated auxin signaling for normal lateral root development in Arabidopsis (Xie et al., 2000; Mallory et al., 2004; Guo et al., 2005; Li et al., 2012). It was shown that auxin responsive miR164 expression provided a homeostatic mechanism to cleave AtNAC1 transcripts, which in turn down regulate auxin signals (Guo et al., 2005). Interestingly, it has been reported that the miRNAs regulating root architecture via modulating auxin signaling can be responsive to drought stress as well (Meng et al., 2010; Gao et al., 2016). An earlier study demonstrated that miR164 may regulate the agedependent cell death and senescence in Arabidopsis leaves. This occurs through a trifurcate feed-forward pathway involving NAC TF ORE1/ AtNAC2, miR164 and ethylene insensitive 2 (EIN2, positive regulator of the ethylene response). In this pathway, miR164 expression gradually decreases with aging through negative regulation by EIN2, which leads to up-regulation of ORE1 expression that ultimately results in the leaf cell death (Kim et al., 2009). Similarly it was shown that ethylene regulates cell expansion by fine-tuning the miRNA164/RhNAC100 module. This has also been associated with cell expansion in Arabidopsis petals. In later stages of flower opening, an increase in ethylene production affects miR164 abundance, resulting in an accumulation of RhNAC100, which restricts cell expansion and slows the rate of petals growth (Pei et al., 2013). 6. Perspective

Acknowledgments

The members of NAC-TF family and the miRNAs have been well characterized for their regulatory roles in different pathways related to plant development and stress responses (Quach et al., 2014; Gonçalves et al., 2015; Yoon et al., 2015; Zhong and Ye, 2015). They comprise of diverse members encoded by large gene families and have a widespread impact on gene expression. This assortment enables them to control adaptation to varying environment conditions (Wang et al., 2013). Although significant progress has been made in understanding the functions of many NAC-TFs and their regulatory miRNA in different plant responses, our knowledge of their function is probably limited by the cellular complexity and modularity. To completely understand their role in regulating the plant responses it is important to identify the expression patterns and interacting partners of the NAC-TFs. Functional analysis of miRNA regulated NAC-TFs show that they are involve in diverse mechanism of development, hormone and stress response. The versatile role of NAC-TFs has identified them as potential candidates for engineering tolerance to environmental stresses. Arabidopsis transgenic lines overexpressing NAC genes (like At-RD26, At-ATAF1, Os-SNAC1, OsNAC6/SNAC2, Os-NAC5) from soybean, Trticum aestivum, Miscanthus and Artemisia annua have been used to improve tolerance to heat, cold, drought, salt and/or diseases (Nakashima et al., 2009; Takasaki et al., 2010; Mao et al., 2014; Quach et al., 2014; Lv et al., 2016; Zhao et al., 2016). There are other positive reports on the generation of stress tolerant transgenics in model plants like rice and tobacco (Jin et al., 2013; Hong et al., 2016). However, the success story may not be universal as NAC homologues may not necessarily activate the specific regulatory pathways in the introduced plant. This discrepancy may be attributed to the functional diversification of the NAC genes following duplication. An excellent example is provided by the LYS14 of Saccharomyces cerevisiae, which is a key activator of four genes involved in lysine biosynthesis, but the

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