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. 2011 Oct 1;6(10):1564–1566. doi: 10.4161/psb.6.10.17003

Signaling linkage between environmental stress resistance and leaf senescence in Arabidopsis

Pil Joon Seo 1, Chung-Mo Park 1,✉
PMCID: PMC3256385  PMID: 21921691

Abstract

Plants possess versatile strategies that permit efficient use of limited nutrient resources during senescing process. This metabolic adjustment is critical for prevention of diverse cellular damage and thus for reproductive success and offspring production, particularly under environmental stress conditions. However, it is largely unknown how age-dependent resistance to cellular damages is established and how it is influenced by environmental stress signals during senescing process. We found that the VNI2 (VND-INTERACTING 2) transcription factor, which belongs to the NAC (NAM/ATAF1, 2/CUC2) transcription factor family, plays a role in the age-dependent induction of stress resistance. The VNI2 transcription factor is transcriptionally induced during senescing process and regulates COR/RD genes by binding directly to their promoters. The COR/RD proteins play a role in the protection from diverse cellular damages during senescing process. Notably, the transcriptional activation activity of VNI2 is further elevated under high salinity. These results indicate that plants increase environmental stress resistance by inducing the VNI2 gene to assure their reproductive success, supporting signaling crosstalk between stress resistance response and senescing process.

Key words: abscisic acid, arabidopsis, COR/RD, salt stress, senescence, VNI2

Leaf Senescence and Environmental Stress Resistance

Leaf senescence, which is the final developmental step of plant life cycle, is orderly and active process.1 The tightly controlled developmental process is particularly important for nutrient recycling and energy redistribution, assuring reproductive success.1–3 Since plants are vulnerable to environmental changes as they age, protection strategies to complete their life cycle and produce offspring are necessary during senescing process,1 especially under environmental stress conditions.

It has been well-known that environmental stress responses and aging process is intimately interconnected.1,3 Increased environmental stress resistance is frequently accompanied by prolonged longevity.4–6 Conversely, mutants that exhibit expanded life span are also resistant to environmental stress. The close relationship between aging process and environmental stress response have been documented extensively in many living organisms such as Drosophila melanogaster, Saccharomyces cerevisiae and Mus musculus.6–10 In Arabidopsis, numerous senescence-associated genes (SAGs) have been identified,1 and some of them have been shown to be responsive to various environmental stresses, suggesting that environmental stress resistance and leaf senescence are interrelated. However, the underlying molecular mechanisms linking environmental stress regulation and leaf senescence are largely unknown.

The Arabidopsis VNI2 gene encoding a member of NAC transcription factor is induced by salt stress and senescing process,11 suggesting a role of VNI2 as a signaling web between salt stress resistance and leaf senescence. Whereas transgenic plants overexpressing the VNI2 gene (35S:VNI2) exhibit prolonged leaf longevity with enhanced resistance to high salinity, the VNI2-deficient vni2-1 mutant shows accelerated leaf senescence. It is also susceptible to high salinity. Extensive gene expressional analysis revealed that expression of stress-responsive genes is greatly altered but that of SAGs is uninfluenced in the 35S:VNI2 transgenic and vni2-1 mutant plants. In particular, the VNI2 transcription factor regulates COR15A/B and RD29A/B genes by binding directly to their promoters.

The COR15A/B and RD29A/B genes are well-known marker genes that are involved in abiotic stress responses.12,13 The promoters of the COR/RD genes have multiple cis-acting elements that are responsive to diverse stress signals, such as osmotic stress, drought and high salinity. Despite their importance in environmental stress responses, the COR/RD genes have not been explored in leaf senescence. Expression of the COR/RD genes gradually increases as plants senesce.11 Notably, transgenic plants overexpressing either the COR15A/B or RD29A/B genes also exhibit prolonged leaf longevity, indicating that the COR/RD genes play a role in leaf senescence. In nature, plants encounter diverse environmental stress conditions during senescing process. It is well known that environmental resistance correlates with senescing periods.4–6 Whereas leaf longevity is prolonged in stress-resistant plants,14–16 premature senescence occurs in stress-susceptible plants.17 Since longer senescing period contributes to reproductive success, it seems that plants have evolved a physiological mechanism that induces stress resistance as they grow old (Fig. 1).

Figure 1.

Figure 1

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Proposed working model of VNI2 in the regulation of leaf senescence under high salinity. The VNI2 gene is transcriptionally induced during leaf senescing process. The VNI2 transcription factor regulates the COR/RD genes by binding to their gene promoters. The COR/RD proteins play a role in the protection of leaf cells from diverse cellular damages, establishing age-dependent stress resistance. The transcriptional activation activity of VNI2 is also modulated by salt stress, linking plant salt stress resistance to leaf senescence.

Modulation of Transcriptional Regulation Activity of VNI2 by High Salinity

Transcription factor activity is regulated at multiple steps: transcription, chromatin modification, posttranscriptional RNA metabolism, modulation of subcellular localization, dynamic dimer formation and posttranslational chemical modification.18

Modulation of transcriptional regulation activity is also an intriguing mechanism regulating transcription factor activity.19,20 The VNI2 transcription factor has been previously reported as a transcriptional repressor.21 We also found that VNI2 acts as a transcriptional repressor under normal growth conditions. The VNI2 transcription factor possesses a transcriptional activation domain in the C-terminal region. Notably, the transcriptional activation activity is modulated by environmental stresses, such as high salinity. It has been demonstrated that the VNI2 transcription factor behaves as a transcription activator under high salinity, providing a new layer of transcriptional regulation. It is apparent that the transcriptional regulation activity of VNI2 is also modulated through interactions with cis-acting elements. Transient expression assays using Arabidopsis protoplasts revealed that the VNI2 transcription factor binds directly to the promoters of the COR and RD genes and activates their transcription even under normal growth conditions. Consistently, the COR and RD genes are upregulated in the 35S:VNI2 transgenic plants. These observations indicate that the transcriptional regulation activity of VNI2 is influenced by environmental stress as well as by specific interactions with cis-acting elements in the promoters of target genes.

The VNI2 gene is also regulated developmentally through senescing process. Therefore, the regulation of the COR/RD genes by VNI2 is age-dependent. When environmental stress is applied to senescing plants, the VNI2 activity is further elevated by increasing the transcriptional activation activity. Regulation of the transcriptional regulation activity is certainly a direct and rapid way of responding efficiently to incoming environmental fluctuations, ensuring reproductive success under environmental stress conditions without premature death.

Acknowledgments

This work was supported by the Leaping Research Program (20100014373) provided by the National Research Foundation of Korea and by grants from the Plant Signaling Network Research Center (20100001457), the National Research Foundation of Korea (20100028147), and from the Next-Generation BioGreen 21 program (Plant Molecular Breeding Center No. PJ008103), Rural Development Administration, Republic of Korea.

Addendum to: Yang SD, Seo PJ, Yoon HK, Park CM. The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell. 2011;23:2155–2168. doi: 10.1105/tpc.111.084913.

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