Abstract
Key message
RGA/GAI and NAP interacted with each other, and NAP was involved in GA signaling as a role of regulating age-dependent and dark-induced leaf senescence in Arabidopsis.
Abstract
Leaf senescence is a significant biological process which is beneficial for plant growth, development, and generation alternation in Arabidopsis. Recent researches have shown gibberellins (GAs) could accelerate leaf senescence. Nevertheless, the GA signaling involved in leaf senescence process remains elusive. Here, we reported a new potential regulation mechanism of GA-mediated chlorophyll degradation and leaf senescence. In this study, we confirmed that NAP positively regulated age-dependent and dark-induced leaf senescence and NAP knockout mutant nap was hyposensitive to GA3 (an active form of GA) treatment. DELLA family proteins with highly conserved structural domain function as master growth repressors that integrated GA signaling and leaf senescence. We validated RGA and GAI could interact with NAP in vitro and in vivo, and subsequently impaired the transcriptional activities of NAP to induce SAG113 and AAO3 expression in nap protoplasts. Taken together, we suggest that NAP is a novel component of the regulatory network that modulates the progress of leaf senescence in GA signaling.
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Abbreviations
- NAP-OX :
-
NAP overexpression
- BiFC:
-
Bimolecular fluorescence complementation
- fLUC:
-
Firefly luciferase
- GA:
-
Gibberellin
- GAI :
-
GA-insensitive
- RGA :
-
Repressor of ga1-3
- RGL1 :
-
RGA-like 1
- RGL2 :
-
RGA-like 2
- RGL3 :
-
RGA-like 3
- NYC1 :
-
Non-yellow coloring 1
- PAC:
-
Paclobutrazol
- qRT-PCR:
-
Real-time quantitative reverse
References
Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Huaming C, Paul S, Stevenson DK, Justin Z, Pascual B, Rosa C (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657
Breeze E, Harrison E, Mchattie S, Hughes L, Hickman R, Hill C (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894
Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585
Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2010) The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol J 1:3–22
Chen Y, Qiu K, Kuai B, Ding Y (2011) Identification of an NAP-like transcription factor BeNAC1 regulating leaf senescence in bamboo (Bambusa emeiensis ‘Viridiflavus’). Physiol Plant 142:361–371
Chen M, Maodzeka A, Zhou L, Ali E, Zhong W, Jiang L (2014) Removal of DELLA repression promotes leaf senescence in Arabidopsis. Plant Sci 219–220:26–34
Chen L, Xiang S, Chen Y, Li D, Yu D (2017) Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence. Mol Plant 10:1174–1189
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17
Davière JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151
Davière JM, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9:10–20
De Lucas M, Davière J-M, Rodríguez Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484
Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479
Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9:1272–1285
Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112
Guo Y, Gan S (2010) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612
Hedden P (2001) Gibberellin metabolism and its regulation. J Plant Growth Regul 20:317–318
Hong G-J, Xue X-Y, Mao Y-B, Wang L-J, Chen X-Y (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648
Kalivas A, Pasentsis K, Argiriou A, Tsaftaris AS (2010) Isolation, characterization, and expression analysis of an NAP-Like cDNA from Crocus (Crocus sativus L.). Plant Mol Biol Rep 28:654–663
Li H, Lin F, Gui W, Jing R, Qi Z, Li Z (2012) Quantitative trait loci mapping of dark-induced senescence in winter wheat (Triticum aestivum). J Integr Plant Biol 54:33–44
Lim PO, Kim HJ, Hong GN (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
Liu X, Li Z, Jiang Z, Zhao Y, Peng J, Jin J, Guo H, Luo J (2011) LSD: a leaf senescence database. Nucleic Acids Res 39:D1103–D1107
Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247
Ren G, Qian Z, Wu S, Zhang Y, Zhang L, Huang J, Sun Z, Kuai B (2010) Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J Integr Plant Biol 52:496–504
Ren T, Wang J, Zhao M, Gong X, Wang S, Wang G, Zhou C (2017) Involvement of NAC transcription factor SiNAC1 in a positive feedback loop via ABA biosynthesis and leaf senescence in foxtail millet. Planta 247:1–16
Riechmann JL, Ratcliffe OJ (2000) A genomic perspective on plant transcription factors. Curr Opin Plant Biol 3:423–434
Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103
Sakuraba Y, Jeong J, Kang MY, Kim J, Paek NC, Choi G (2014) Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun 5:4636
Schwechheimer C (2011) Gibberellin signaling in plants—the extended version. Front Plant Sci 2:107
Schwechheimer C, Zourelidou M, Bevan MW (1998) Plant transcription factor studies. Annu Rev Plant Physiol Plant Mol Biol 49:127–150
Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198
Ülker B, Mukhtar MS, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226:125–137
Van Der Graaff E, Schwacke R, Schneider A, Desimone M, Flügge U-I, Kunze R (2006) Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792
Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS (2009) Tape-Arabidopsis sandwich—a simpler Arabidopsis protoplast isolation method. Plant Methods 5:16
Yamaguchi S (2001) Gibberellin metabolism and its regulation. J Plant Growth Regul 20:317–318
Yang J, Worley E, Udvardi M (2014) A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell 26:4862–4874
Yin Y, Wang ZY, Mora Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191
Yoo S-D, Cho Y-H, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Zhang K, Gan S-S (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158:961–969
Zhang H, Zhou C (2013) Signal transduction in leaf senescence. Plant Mol Biol 82:539–545
Zhang DW, Xu F, Zhang ZW, Chen YE, Du JB, Jia SD, Yuan S, Lin HH (2010) Effects of light on cyanide-resistant respiration and alternative oxidase function in Arabidopsis seedlings. Plant, Cell Environ 33:2121–2131
Zhang Y, Liu Z, Chen Y, He J, Bi Y (2015) PHYTOCHROME-INTERACTING FACTOR 5 (PIF5) positively regulates dark-induced senescence and chlorophyll degradation in Arabidopsis. Plant Sci 237:57–68
Zhang Y, Liu Z, Liu J, Lin S, Wang J, Lin W, Xu W (2017) GA-DELLA pathway is involved in regulation of nitrogen deficiency-induced anthocyanin accumulation. Plant Cell Rep 36:557–569
Zhang Y, Liu Z, Wang X, Wang J, Fan K, Li Z, Lin W (2018) DELLA proteins negatively regulate dark-induced senescence and chlorophyll degradation in Arabidopsis through interaction with the transcription factor WRKY6. Plant Cell Rep 2018:1–12
Zhou C, Cai Z, Guo Y, Gan S (2009) An arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150:167–177
Zhu T, Nevo E, Sun D, Peng J (2012) Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66:1833–1848
Funding
This work was supported by the National Basic Research Program of China (973 Program) (2015CB150100), the National Natural Science Foundation of China (31670235 and 31970263 to HL; 31570237 to DZ), the National Research and Development Project of Transgenic Crops of China (2016ZX08009-003-002), Sichuan Natural Science Foundation (2019YFS0457) and Forage Innovation Team Supporting Fund from Sichuan Provincial Department of Agriculture, the Fundamental Research Funds for the Central Universities (SCU2019D013, SCU2018D006)
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Communicated by Inhwan Hwang.
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Lei, W., Li, Y., Yao, X. et al. NAP is involved in GA-mediated chlorophyll degradation and leaf senescence by interacting with DELLAs in Arabidopsis. Plant Cell Rep 39, 75–87 (2020). https://doi.org/10.1007/s00299-019-02474-2
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DOI: https://doi.org/10.1007/s00299-019-02474-2