Roles of stay-green (SGR) homologs during chlorophyll degradation in green plants

Armstead I, Donnison I, Aubry S, Harper J, Hortensteiner S, James C, Mani J, Moffet M, Ougham H, Roberts L, Thomas A, Weeden N, Thomas H, King I (2007) Cross-species identification of Mendel’s I locus. Science 315(5808):73 Aubry S, Mani J, Hortensteiner S (2008) Stay-green protein, defective in Mendel’s green cotyledon mutant, acts independent and upstream of pheophorbide a oxygenase in the chlorophyll catabolic pathway. Plant Mol Biol 67(3):243–256 Barry CS, McQuinn RP, Chung MY, Besuden A, Giovannoni JJ (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147(1):179–187 Biswal B (1995) Carotenoid catabolism during leaf senescence and its control by light. J Photochem Photobiol B Biol 30:3–13 Borovsky Y, Paran I (2008) Chlorophyll breakdown during pepper fruit ripening in the chlorophyll retainer mutation is impaired at the homolog of the senescence-inducible stay-green gene. Theor Appl Genet 117(2):235–240 Chen J, Ren G, Kuai B (2016) The mystery of Mendel’s stay-green: magnesium stays chelated in chlorophylls. Mol Plant 9(12):1556–1558 Chen Y, Shimoda Y, Yokono M, Ito H, Tanaka A (2018) Mg-dechelatase is involved in the formation of photosystem II but not in chlorophyll degradation in Chlamydomonas reinhardtii. Plant J 97:1022–1031 Christ B, Schelbert S, Aubry S, Sussenbacher I, Muller T, Krautler B, Hortensteiner S (2012) MES16, a member of the methylesterase protein family, specifically demethylates fluorescent chlorophyll catabolites during chlorophyll breakdown in Arabidopsis. Plant Physiol 158(2):628–641 Christ B, Egert A, Sussenbacher I, Krautler B, Bartels D, Peters S, Hortensteiner S (2014) Water deficit induces chlorophyll degradation via the ‘PAO/phyllobilin’ pathway in leaves of homoio- (Craterostigma pumilum) and poikilochlorophyllous (Xerophyta viscosa) resurrection plants. Plant Cell Environ 37(11):2521–2531 Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JG, McCourt P, Samuel MA (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proc Natl Acad Sci USA 110(40):E3888–3894 Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (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(9):1272–1285 Hauenstein M, Christ B, Das A, Aubry S, Hortensteiner S (2016) A role for TIC55 as a hydroxylase of phyllobilins, the products of chlorophyll breakdown during plant senescence. Plant Cell 28(10):2510–2527 Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77 Hortensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Cell 14(3):155–162 Hu ZL, Deng L, Yan B, Pan Y, Luo M, Chen XQ, Hu TZ, Chen GP (2011) Silencing of the LeSGR1 gene in tomato inhibits chlorophyll degradation and exhibits a stay-green phenotype. Biol Plant 55(1):27–34 Jiang H, Li M, Liang N, Yan H, Wei Y, Xu X, Liu J, Xu Z, Chen F, Wu G (2007) Molecular cloning and function analysis of the stay green gene in rice. Plant J 52(2):197–209 Jiang H, Chen Y, Li M, Xu X, Wu G (2011) Overexpression of SGR results in oxidative stress and lesion-mimic cell death in rice seedlings. J Integr Plant Biol 53(5):375–387 Kuai B, Chen J, Hortensteiner S (2018) The biochemistry and molecular biology of chlorophyll breakdown. J Exp Bot 69(4):751–767 Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M, Tanaka A (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19(4):1362–1375 Li Z, Wu S, Chen J, Wang X, Gao J, Ren G, Kuai B (2017) NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis. Plant J 92(4):650–661 Luo Z, Zhang J, Li J, Yang C, Wang T, Ouyang B, Li H, Giovannoni J, Ye Z (2013) A STAY-GREEN protein SlSGR1 regulates lycopene and beta-carotene accumulation by interacting directly with SlPSY1 during ripening processes in tomato. New Phytol 198(2):442–452 Matile P, Hourtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95 Matsuda K, Shimoda Y, Tanaka A, Ito H (2016) Chlorophyll a is a favorable substrate for Chlamydomonas Mg-dechelatase encoded by STAY-GREEN. Plant Physiol Biochem 109:365–373 Mecey C, Hauck P, Trapp M, Pumplin N, Plovanich A, Yao J, He SY (2011) A critical role of STAYGREEN/Mendel’s I locus in controlling disease symptom development during Pseudomonas syringae pv tomato infection of Arabidopsis. Plant Physiol 157(4):1965–1974 Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23(9):3442–3453 Mendel G (1866) Versuche über pflanzenhybriden. Verhandlungen des naturforschenden Vereines in Brünn 4:3–47 Ming N, Ma NN, Jiao BZ, Lv W, Meng QW (2020) Genome wide identification of C2H2-type zinc finger proteins of tomato and expression analysis under different abiotic stresses. Plant Mol Biol Rep 38:75–94 Park SY, Yu JW, Park JS, Li J, Yoo SC, Lee NY, Lee SK, Jeong SW, Seo HS, Koh HJ, Jeon JS, Park YI, Paek NC (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19(5):1649–1664 Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci USA 100(25):15259–15264 Pruzinska A, Anders I, Aubry S, Schenk N, Tapernoux-Luthi E, Muller T, Krautler B, Hortensteiner S (2007) In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19(1):369–387 Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H, Ge X, Kuai B (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol 144(3):1429–1441 Rong H, Tang Y, Zhang H, Wu P, Chen Y, Li M, Wu G, Jiang H (2013) The Stay-Green Rice like (SGRL) gene regulates chlorophyll degradation in rice. J Plant Physiol 170(15):1367–1373 Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andres CB, Kessler F, Hortensteiner S, Paek NC (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24(2):507–518 Sakuraba Y, Park SY, Kim YS, Wang SH, Yoo SC, Hortensteiner S, Paek NC (2014a) Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence. Mol Plant 7(8):1288–1302 Sakuraba Y, Kim D, Kim YS, Hortensteiner S, Paek NC (2014b) Arabidopsis STAYGREEN-LIKE (SGRL) promotes abiotic stress-induced leaf yellowing during vegetative growth. FEBS Lett 588(21):3830–3837 Sakuraba Y, Jeong J, Kang MY, Kim J, Paek NC, Choi G (2014c) Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun 5:4636 Sato Y, Morita R, Nishimura M, Yamaguchi H, Kusaba M (2007) Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc Natl Acad Sci USA 104(35):14169–14174 Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hortensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21(3):767–785 Shimoda Y, Ito H, Tanaka A (2016) Arabidopsis STAY-GREEN, Mendel’s green cotyledon gene, encodes magnesium-dechelatase. Plant Cell 28:2147–2160 Vom Dorp K, Holzl G, Plohmann C, Eisenhut M, Abraham M, Weber APM, Hanson AD, Dormann P (2015) Remobilization of phytol from chlorophyll degradation is essential for to copherol synthesis and growth of Arabidopsis. Plant Cell 27:2846–2859 Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2(8):e718 Wu S, Li Z, Yang L, Xie Z, Chen J, Zhang W, Liu T, Gao S, Gao J, Zhu Y, Xin J, Ren G, Kuai B (2016) NON-YELLOWING2 (NYE2), a close paralog of NYE1, plays a positive role in chlorohyll degradation in Arabidopsis. Mol Plant 9(4):624–627 Xie Z, Wu S, Chen J, Zhu X, Zhou X, Hortensteiner S, Ren G, Kuai B (2019) The C-terminal cysteine-rich motif of NYE1/SGR1 is indispensable for its function in chlorophyll degradation in Arabidopsis. Plant Mol Biol 101(3):257–268 Zhang TT, Lv W, Zhang HS, Ma L, Li PH, Ge L, Li G (2018) Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize. BMC Plant Biol 18:235 Zhou C, Han L, Pislariu C, Nakashima J, Fu C, Jiang Q, Quan L, Blancaflor EB, Tang Y, Bouton JH, Udvardi M, Xia G, Wang ZY (2011) From model to crop: functional analysis of a STAY-GREEN gene in the model legume Medicago truncatula and effective use of the gene for alfalfa improvement. Plant Physiol 157(3):1483–1496