Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis

Journal of Experimental Botany, Jul 2014

After germination, cotyledons undertake the major role in supplying nutrients to the pre-photoautorophy angiosperm seedlings until they senesce. Like other senescence processes, cotyledon senescence is a programmed degenerative process. Nitric oxide can induce premature cotyledon senescence in Arabidopsis thaliana, yet the underlying mechanism remains elusive. A screen for genetic mutants identified the nes1 mutant, in which cotyledon senescence was accelerated by nitric oxide. Map-based cloning revealed that NES1 is allelic to a previously reported mitotic checkpoint family gene, MAD1. The nes1/mad1 mutants were restored to the wild type, in response to nitric oxide, by transforming them with pNES1::NES1. Ectopic expression of NES1 in the wild type delayed nitric oxide-mediated cotyledon senescence, confirming the repressive role of NES1. Moreover, two positive regulators of leaf senescence, the ethylene signalling component EIN2 and the transcription factor ORE1/AtNAC2/ANAC092, were found to function during nitric oxide-induced senescence in cotyledons. The block of ORE1 function delayed senescence and ectopic expression induced the process, revealing the positive role of ORE1. EIN2 was required to induce ORE1. Furthermore, the genetic interaction analysis between NES1 and ORE1 showed that the ore1 loss-of-function mutants were epistatic to nes1, suggesting the dominant role of ORE1 and the antagonistic role of NES1 during nitric oxide-induced cotyledon senescence in Arabidopsis.

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Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis

Journal of Experimental Botany Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis Jing Du 2 Manli Li 2 Dongdong Kong 1 Lei Wang 2 Qiang Lv 2 Jinzheng Wang 2 Fang Bao 2 Qingqiu Gong 0 Jinchan Xia 2 Yikun He 2 0 College of Life Sciences, Nankai University , Tianjin, 300071 , PR China 1 Department of Cell Biology and Molecular Genetics, University of Maryland , College Park, MD 20742 , USA 2 College of Life Sciences, Capital Normal University , Beijing, 100048 , PR China After germination, cotyledons undertake the major role in supplying nutrients to the pre-photoautorophy angiosperm seedlings until they senesce. Like other senescence processes, cotyledon senescence is a programmed degenerative process. Nitric oxide can induce premature cotyledon senescence in Arabidopsis thaliana, yet the underlying mechanism remains elusive. A screen for genetic mutants identified the nes1 mutant, in which cotyledon senescence was accelerated by nitric oxide. Map-based cloning revealed that NES1 is allelic to a previously reported mitotic checkpoint family gene, MAD1. The nes1/mad1 mutants were restored to the wild type, in response to nitric oxide, by transforming them with pNES1::NES1. Ectopic expression of NES1 in the wild type delayed nitric oxide-mediated cotyledon senescence, confirming the repressive role of NES1. Moreover, two positive regulators of leaf senescence, the ethylene signalling component EIN2 and the transcription factor ORE1/AtNAC2/ANAC092, were found to function during nitric oxide-induced senescence in cotyledons. The block of ORE1 function delayed senescence and ectopic expression induced the process, revealing the positive role of ORE1. EIN2 was required to induce ORE1. Furthermore, the genetic interaction analysis between NES1 and ORE1 showed that the ore1 loss-of-function mutants were epistatic to nes1, suggesting the dominant role of ORE1 and the antagonistic role of NES1 during nitric oxide-induced cotyledon senescence in Arabidopsis. Rch aep; Arabidopsis; cotyledon; induced senescence; NES1/MAD1; nitric oxide; ORE1/AtNAC2 - Cotyledons are formed during embryogenesis. In most plants, the function of the cotyledon is to provide nutrients for seedling establishment. During seedling development, the cotyledon is initially heterotrophic, then becomes photosynthetic, and eventually senesces. As an integral part of development, the senescence of cotyledons is a process that leads to nutrient recycling and ends in cell death, and is accompanied by colour changes, the dismantling of chloroplasts, and the degradation of DNA, RNA, and protein (Krul, 1974; Peterman and Siedow, 1985). Phytohormones such as cytokinin and ethylene affect cotyledon senescence, with cytokinin preventing chlorophyll breakdown and ethylene initiating the onset of the senescence process (Ananieva et al., 2008a; Jing et al., 2008). Although cotyledon senescence has been studied for decades (McKersie et al., 1987; Rukes and Mulkey, 1993), its underlying regulatory network is unclear. In contrast, leaf senescence is better understood (Lim et al., 2007). Based on transcriptome analysis, during natural leaf senescence, ~6–12% of Arabidopsis genes change expression (Buchanan-Wollaston et al., 2005; Breeze et al., 2011), which © The Author 2013. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. include >800 SAGs (senescence-associated genes). A number of SAGs have been well studied and established as markers. The favoured marker for monitoring age-dependent senescence is SAG12, whereas SAG13 and SAG14 are preferred for monitoring stress-induced senescence (Schippers et  al., 2007). Nevertheless, deletion or overexpression of many individual SAGs affect senescence to a limited extent, although there are a few exceptions (Seo et al., 2011; Zhang and Gan, 2012), indicating the robust nature of the regulatory network. Certain transcription factors have been identified as positive regulators of age-dependent senescence in Arabidopsis by means of the loss-of-function mutant experiencing delayed leaf senescence, whereas others have been identified as negative regulators, in this case based on accelerated senescence in the loss-of-function mutant. The better known positive regulators of leaf senescence are from the NAC (NAM, ATAF, and CUC) family. So far, a few have been well characterized, including AtNAP (Arabidopsis NAC domain containing protein 29)  and ORE1/AtNAC2/ANAC092 (ORESARA1). Not only does a block of function delay senescence, but ectopic expression induces early senescence (Guo and Gan, 2006; Rauf et al., 2013). The control o (...truncated)


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Jing Du, Manli Li, Dongdong Kong, Lei Wang, Qiang Lv, Jinzheng Wang, Fang Bao, Qingqiu Gong, Jinchan Xia, Yikun He. Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis, Journal of Experimental Botany, 2014, pp. 4051-4063, 65/14, DOI: 10.1093/jxb/ert429