Regulatory network of NAC transcription factors in leaf senescence
Introduction
Leaves undergo developmental and physiological changes during their lifespan, ending with senescence and death [1]. Leaf senescence is an important developmental phase and considerably impacts crop yields. During senescence, leaves change their role from nutrient-accumulating organs through carbon fixation and nutrient uptake to nutrient-exporting organs, resulting in nutrient recycling to developing organs [1].
Leaf senescence is a part of the plant developmental process but can be triggered by environmental changes that are integrated into the developmental aging program (Figure 1a) [1, 2]. This integrated senescence response determines the pattern of leaf senescence and contributes to improved survival in a given ecological niche.
Temporal profiling of transcripts during leaf senescence in several plants, including Arabidopsis, wheat, barley, and rice, revealed the highly ordered molecular events involving the temporal coordination of the expression of thousands of genes, including those encoding transcription factors (TFs), during aging [3]. NAC, WRKY, and MYB TFs are central players in modulating transcriptional changes during senescence. Recently, key gene regulatory networks comprising these TFs have been identified, indicating that leaf senescence is controlled by multiple and cross-linking pathways, many of which are associated with stress response signaling [4, 5, 6, 7].
In this review, we mainly focus on the recent advances of NAC regulatory networks, which have greatly expanded our understanding on the nature and regulation of leaf senescence. The structural features of NAC TFs, their contributions to form complex networks at multiple levels, and the biological implications of the NAC network are discussed.
Section snippets
NAC transcription factors as key regulators in leaf senescence
NAC proteins are among the largest plant-specific TF superfamily with >100 members in the Arabidopsis genome [8]. This family has expanded during the evolution of land plants, possibly along with the elaborate developmental program critical to maximize plant fitness. NAC TF family members were implicated in the regulation of transcriptional reprogramming associated with diverse developmental processes [9].
As shown in global transcriptome profiling, >30 NAC genes showed enhanced expression
Structural features of NAC TF contributing to complex networks
Typically, NAC proteins exhibit a highly conserved N-terminal NAC domain with DNA-binding and dimerization abilities [16, 17]. The C-terminal region of NAC members is diverse and intrinsically disordered and functions as a transcription regulatory domain (TRD) [18, 19].
Biophysical and crystal structure analyses of A. thaliana ANAC019 NAC domain determined a novel transcription factor fold mainly comprising a twisted β-sheet that allowed binding of DNA as homo-dimers and hetero-dimers through
NAC regulatory network integrating environmental signals into the developmental program
Leaf senescence proceeds with leaf age. However, it is also influenced by external stresses [1]. Understanding of the relationship between environmental responses and leaf senescence is mostly derived by studying senescence response to phytohormones such as abscisic acid (ABA), jasmonic acid (JA), ethylene, and salicylic acid (SA) that are extensively involved in the response to various abiotic and biotic stresses [1].
Genome-wide transcriptome analyses revealed that many NAC family members were
NAC TFs effects on the growth and production of crops
The importance of stress-responsive NAC TFs as central regulators of leaf senescence has been demonstrated in major crops [49, 50, 51]. Overexpression of the stress-inducible SNAC1 gene in rice improved drought and salt tolerance at the vegetative stage, and produced higher seed yield under drought conditions at the productive stage [52]. ABA-induced OsNAP, a rice ortholog of ANAC029/AtNAP, is a key component connecting ABA-signaling and leaf senescence via a feedback regulation of ABA
Conclusion and challenges
Recent advances in NAC TF research have provided valuable insights on the significance of NAC TFs as key players for integrating developmental age information and external environmental signals during plant development. Particularly, NAC TF mechanisms for senescence regulation are dissected by identifying the upstream regulators of NAC genes, their downstream target genes, and interacting partners to link stress-related signaling with senescence-related transcriptional cascades. Features of
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was supported by the Institute for Basic Science [IBS-R013-D1], the DGIST R&D Program [15-HRLA-01], and Basic Science Research Program [2010-0010915] funded by the Ministry of Science.
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