The roles of tetrapyrroles in plastid retrograde signaling and tolerance to environmental stresses
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This review provides new insights that tetrapyrrole signals play important roles in nuclear gene expression, chloroplast development and plant’s resistance to environmental stresses.
Higher plants contain many tetrapyrroles, including chlorophyll (Chl), heme, siroheme, phytochromobilin and some of their precursors, all of which have important biological functions. Genetic and physiological studies indicated that tetrapyrrole (mainly Mg-protoporphyrin IX) retrograde signals control photosynthesis-associated nuclear gene (PhANG) expression. Recent studies have shown that tetrapyrrole-derived signals may correlate with plant resistance to environmental stresses such as drought, high-light stress, water stress, osmotic stress, salinity and heavy metals. Signaling and physiological roles of Mg-protoIX-binding proteins (such as PAPP5, CRD and HSP90) and heme-binding proteins (such as HO and TSPO) and tetrapyrrole-signaling components (such as GUN1, ABI4 and CBFA) are summarized. Some of them positively regulate plant development and response to environmental stresses. The intermediate signaling components (such as PTM, HSP70–HSP90–HAP1 complex and PAPP5) between the nucleus and the plastid also positively regulate plant resistance to environmental stresses. This review provides new insights that genetically modified plants with enhanced tetrapyrrole levels have improved resistance to environmental stresses.
KeywordsMg-protoIX Heme GUN Environmental stresses Plastid retrograde signaling
This work was supported by the Sichuan Natural Science Foundation (13ZB0296 and 014z1700), the Preeminent Youth Fund of Sichuan Province (2015JQO045) and the National Natural Science Foundation of China (31300207). We thank LetPub for its linguistic assistance during the preparation of this manuscript and Dr. Ming Yuan (Sichuan Agricultural University) for helpful discussion.
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Conflict of interest
The authors declare that they have no conflict of interest.
- Cheng J, He CX, Zhang ZW, Xu F, Zhang DW, Wang X, Yuan S, Lin HH (2011) Plastid signals confer Arabidopsis tolerance to water stress. Z Naturforsch 66c:47–54Google Scholar
- Duanmu D, Casero D, Dent RM, Gallaher S, Yang W, Rockwell NC, Martin SS, Pellegrini M, Niyogi KK, Merchant SS, Grossman AR, Lagarias JC (2013) Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc Natl Acad Sci USA 110:3621–3626PubMedCentralCrossRefPubMedGoogle Scholar
- Enami K, Ozawa T, Motohashi N, Nakamura M, Tanaka K, Hanaoka M (2011) Plastid-to-nucleus retrograde signals are essential for the expression of nuclear starch biosynthesis genes during amyloplast differentiation in tobacco BY-2 cultured cells. Plant Physiol 157:518–530PubMedCentralCrossRefPubMedGoogle Scholar
- Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012PubMedCentralCrossRefPubMedGoogle Scholar
- Gläßer C, Haberer G, Finkemeier I, Pfannschmidt T, Kleine T, Leister D, Dietz KJ, Häusler RE, Grimm B, Mayer KF (2014) Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core Module of genes embedded in complex cellular signaling networks. Mol Plant 7:1167–1190CrossRefPubMedGoogle Scholar
- Lee KP, Kim C, Landgraf F, Apel K (2008) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 87:10270–10275Google Scholar
- Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785PubMedCentralCrossRefPubMedGoogle Scholar
- Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedCentralPubMedGoogle Scholar
- Reinbothe C, Lebedev N, Reinbothe S (1999) A protochlorophyllide light-harvesting complex involved in de-etiolation of higher plants Nature 397:80–84Google Scholar
- Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935PubMedCentralCrossRefPubMedGoogle Scholar
- Voigt C, Oster U, Börnke F, Jahns P, Dietz KJ, Leister D, Kleine T (2010) In-depth analysis of the distinctive effects of norflurazon implies that tetrapyrrole biosynthesis, organellar gene expression and ABA cooperate in the GUN-type of plastid signaling. Physiol Plant 138:503–519CrossRefPubMedGoogle Scholar
- Wang P, Wan C, Xu Z, Wang P, Wang W, Sun C, Ma X, Xiao Y, Zhu J, Gao X, Deng X (2013) One divinyl reductase reduces the 8-vinyl groups in various intermediates of chlorophyll biosynthesis in a given higher plant species, but the isozyme differs between species. Plant Physiol 161:521–534PubMedCentralCrossRefPubMedGoogle Scholar
- Xie Y, Ling T, Han Y, Liu K, Zheng Q, Huang L, Yuan X, He Z, Hu B, Fang L, Shen Z, Yang Q, Shen W (2008) Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell and Environ 31:1864–1881CrossRefGoogle Scholar