[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.14348/molcells.2015.0039

The Divergent Roles of STAYGREEN (SGR) Homologs in Chlorophyll Degradation

Sakuraba, Yasuhito (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University)
Park, So-Yon (Department of Plant Pathology, Physiology and Weed Science)
Paek, Nam-Chon (Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University)

Abstract

Degradation of chlorophyll (Chl) by Chl catabolic enzymes (CCEs) causes the loss of green color that typically occurs during senescence of leaves. In addition to CCEs, STAYGREEN1 (SGR1) functions as a key regulator of Chl degradation. Although sgr1 mutants in many plant species exhibit a staygreen phenotype, the biochemical function of the SGR1 protein remains elusive. Many recent studies have examined the physiological and molecular roles of SGR1 and its homologs (SGR2 and SGR-LIKE) in Chl metabolism, finding that these proteins have different roles in different species. In this review, we summarize the recent studies on SGR and discuss the most likely functions of SGR homologs.

Keywords

abiotic stress; chlorophyll catabolic enzymes; chlorophyll degradation; STAYGREEN (SGR); SGR-LIKE (SGRL);

Citations & Related Records

Reference

1	Hirashima, M., Tanaka, R., and Tanaka, A. (2009). Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol. 50, 719-729. DOI ScienceOn
2	Horie, Y., Ito, H., Kusaba, M., Tanaka, R., and Tanaka, A. (2009). Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J. Biol. Chem. 284, 17449-17456. DOI ScienceOn
3	Hortensteiner, S. (2009). Stay-green regulates chlorophyll and chlorophyll- binding protein degradation during senescence. Trends Plant Sci. 14, 155-162. DOI ScienceOn
4	Hortensteiner, S., and Krautler, B. (2011). Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807, 977-988. DOI ScienceOn
5	Huang, W., Chen, Q., Zhu, Y., Hu, F., Zhang, L., Ma, Z., He, Z., and Huang, J. (2013). Arabidopsis thylakoid formation 1 is a critical regulator for dynamics of PSII-LHCII complexes in leaf senescence and excess light. Mol. Plant 6, 1673-1691 DOI ScienceOn
6	Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and Parcy, F. (2002). bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106-111. DOI ScienceOn
7	Jiang, H., Li, M., Liang, N., Yan, H., Wei, Y., Xu, X., Liu, J., Xu, Z., Chen, F., and Wu, G. (2007). Molecular cloning and function analysis of the stay green gene in rice. Plant J. 52, 197-209. DOI ScienceOn
8	Jiang, H., Chen, Y., Li, M., Xu, X., and Wu, G. (2011). Overexpression of SGR results in oxidative stress and lesion-mimic cell death in rice seedlings. J. Integr. Plant Biol. 253, 375-387.
9	Johnson-Flanagan, A.M., and Spencer, M.S. (1994). Ethylene production during development of mustard (Brassica juncea) and canola (Brassica napus) seed. Plant Physiol. 106, 601-606. DOI
10	Kato, Y., and Sakamoto W. (2009). Protein quality control in chloroplast: a current model of D1 protein degradation in the photosystem II repair cycle. J. Biochem. 146, 463-469. DOI ScienceOn
11	Koornneef, M., Hanhart, C.J., Hilhorst, H.W., and Karssen, C.M. (1989). In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol. 90, 463-469. DOI ScienceOn
12	Kusaba, M., Ito, H., Morita, R., Iida, S., Sato, Y., Fujimoto, M., Kawasaki, S., Tanaka, R., Hirochika, H., Nishimura, M., et al. (2007). Rice NON-YELLOW COLORING1 is involved in lightharvesting complex II and grana degradation during leaf senescence. Plant Cell 19, 1362-1375. DOI ScienceOn
13	Liang, C., Wang, Y., Zhu, Y., Tang, J., Hu, B., Liu, L., Ou, S., Wu, H., Sun, X., Chu, J., et al. (2014). OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc. Natl. Acad. Sci. U.S.A. 111, 10013-10018. DOI ScienceOn
14	Lim, P.O., Kim, H.J., and Nam, H.G. (2007). Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136. DOI ScienceOn
15	Luo, Z., Zhang, J., Li, J., Yang, C., Wang, T., Ouyang, B., Li, H., Giovannoni, J., and 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, 442-452. DOI ScienceOn
16	Morita, R., Sato, Y., Masuda, Y., Nishimura, M., and Kusaba, M. (2009). Defect in non-yellow coloring 3, an alpha/beta hydrolase- fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J. 59, 940-952. DOI ScienceOn
17	Mach, J.M., Castillo, A.R., Hoogstraten, R., and Greenberg, J.T. (2001). The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. U.S.A. 98, 771-776. DOI
18	Mecey, C., Hauck, P., Trapp, M., Pumplin, N., Plovanich, A., Yao, J., and He, S.Y. (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, 1965-1974. DOI
19	Meguro, M., Ito, H., Takabayashi, A., Tanaka, R., and Tanaka, A. (2011). Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23, 3442-3453. DOI ScienceOn
20	Nakagawara, E., Sakuraba, Y., Yamasato, A., Tanaka, R., and Tanaka, A. (2007). Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J. 49, 800-809 DOI ScienceOn
21	Nakajima, S., Ito, H., Tanaka, R., and Tanaka, A. (2012). Chlorophyll b reductase plays an essential role in maturation and storability of Arabidopsis seeds. Plant Physiol. 160, 261-273. DOI
22	Olinares, P.D., Kim, J., and van Wijk, K.J. (2011). The Clp protease system; a central component of the chloroplast protease network. Biochim. Biophys. Acta 1807, 999-1011. DOI ScienceOn
23	Ren, G., An, K., Liao, Y., Zhou, X., Cao, Y., Zhao, H., Ge, X., and Kuai, B. (2007). Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 144, 1429-1441. DOI ScienceOn
24	Park, S.Y., Yu, J.W., Park, J.S., Li, J., Yoo, S.C., Lee, N.Y., Lee, S.K., Jeong, S.W., Seo, H.S., Koh, H.J., et al. (2007). The senescence- induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649-1664. DOI ScienceOn
25	Pruzinska, A., Tanner, G., Anders, I., Roca, M., and 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. U.S.A. 100, 15259-15264. DOI ScienceOn
26	Pruzinskz, A., Anders, I., Aubry, S., Schenk, N., Tapernoux-Luthi, E., Muller, T., Krautler, B., and Hortensteiner, S. (2007). In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19, 369-387. DOI ScienceOn
27	Rong, H., Tang, Y., Zhang, H., Wu, P., Chen, Y., Li, M., Wu, G., and Jiang, H. (2013). The Stay-Green Rice like (SGRL) gene regulates chlorophyll degradation in rice. J. Plant Physiol. 170, 1367-1373. DOI ScienceOn
28	Sakuraba, Y., Schelbert, S., Park, S.Y., Han, S.H., Lee, B.D., Andres, C.B., Kessler, F., Hortensteiner, S., and Paek, N.C. (2012). STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24, 507-518. DOI ScienceOn
29	Sakuraba, Y., Kim, Y.S., Yoo, S.C., Hörtensteiner, S., and Paek, N.C. (2013). 7-Hydroxymethyl chlorophyll a reductase functions in metabolic channeling of chlorophyll breakdown intermediates during leaf senescence. Biochem. Biophys. Res. Commun. 430, 32-37. DOI ScienceOn
30	Sakuraba, Y., Lee, S.H., Kim, Y.S., Park, O.K., Hörtensteiner, S., and Paek, N.C. (2014a). Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. J. Exp. Bot. 65, 3915-3925. DOI ScienceOn
31	Sakuraba, Y., Park, S.Y., Kim, Y.S., Wang, S.H., Yoo, S.C., Hörtensteiner, S., and Paek, N.C. (2014b). Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence. Mol. Plant 7, 1288-1302. DOI ScienceOn
32	Sakuraba, Y., Kim, D., Kim, Y.S., Hortensteiner, S., and Paek, N.C. (2014c). Arabidopsis STAYGREEN-LIKE (SGRL) promotes abiotic stress-induced leaf yellowing during vegetative growth. FEBS Lett. 588, 3830-3837. DOI ScienceOn
33	Sakuraba, Y., Jeong, J., Kang, M.Y., Kim, J., Paek, N.C., and Choi, G. (2014d). Phytochrome-interacting transcription factors PIF4 and PIF5 induced leaf senescence in Arabidopsis. Nat. Commun. 5, 4636.
34	Sato, Y., Morita, R., Katsuma, S., Nishimura, M., Tanaka, A., and Kusaba, M. (2009). Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J. 57, 120-131. DOI ScienceOn
35	Sattler, S.E., Gilliland, L.U., Magallanes-Lundback, M., Pollard, M., and DellaPenna, D. (2004). Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16, 1419-1432. DOI ScienceOn
36	Schelbert, S., Aubry, S., Burla, B., Agne, B., Kessler, F., Krupinska, K., and Hortensteiner, S. (2009). Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21, 767-785. DOI ScienceOn
37	Wang, Q., Sullivan, R.W., Kight, A., Henry, R.L., Huang, J., Jones, A.M., and Korth, K.L. (2004). Deletion of the chloroplastlocalized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol. 136, 3594-3604. DOI ScienceOn
38	Tanaka, R., Hirashima, M., Satoh, S., and Tanaka, A. (2003). The Arabidopsis-accelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of the pheophorbide a oxygenase activity does not lead to the "stay-green" phenotype in Arabidopsis. Plant Cell Physiol. 44, 1266-1274. DOI ScienceOn
39	Tang, Y., Li, M., Chen, Y., Wu, P., Wu, G., and Jiang, H. (2011). Knockdown of OsPAO and OsRCCR1 cause different plant death phenotypes in rice. J. Plant Physiol. 168, 1952-1959. DOI ScienceOn
40	Thomas, H. and Howarth, C.J. (2000). Five ways to stay green. J. Exp. Bot. 51, 329-337. DOI ScienceOn
41	Wei, Q., Guo, Y., and Kuai, B. (2011). Isolation and characterization of a chlorophyll degradation regulatory gene from tall fescue. Plant Cell Rep. 30, 1201-1207. DOI
42	Yamatani, H., Sato, Y., Masuda, Y., Kato, Y., Morita, R., Fukunaga, K., Nagamura, Y., Nishimura, M., Sakamoto, W., Tanaka, A., et al. (2013). NYC4, the rice ortholog of Arabidopsis THF1, is involved in the degradation of chlorophyll - protein complexes during leaf senescence. Plant J. 74, 652-662. DOI ScienceOn
43	Zhang, W., Liu, T., Ren, G., Hörtensteiner, S., Zhou, Y., Cahoon, E.B., and Zhang, C. (2014). Chlorophyll degradation: the tocopherol biosynthesis-related phytol hydrolase in Arabidopsis seeds is still missing. Plant Physiol. 166, 70-79. DOI ScienceOn
44	Chao, W.S., Liu, V., Thomson, W.W., Platt, K., and Walling, L.L. (1995). The impact of chlorophyll-retention mutations, d1d2 and cyt-G1, during embryogeny in soybean. Plant Physiol. 107, 253-262. DOI
45	Zhou, C., Han, L., Pislariu, C., Nakashima, J., Fu, C., Jiang, Q., Quan, L., Blancaflor, E.B., Tang, Y., Bouton, J.H., et al. (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, 1483-1496. DOI ScienceOn
46	Armstead, I., Donnison, I., Aubry, S., Harper, J., Hörtensteiner, S., James, C., Mani, J., Moffet, M., Ougham, H., Roberts, L., et al. (2007). Cross-species identification of Mendel's/locus. Science 315, 73. DOI ScienceOn
47	Barry, C.S., McQuinn, R.P., Chung, M.Y., Besuden, A., and Giovannoni, J.J. (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, 179-187. DOI ScienceOn
48	Biswal, B. (1995). Carotenoid catabolism during leaf senescence and its control by light. J. Photochem. Photobiol. B, Biol. 30, 3-13. DOI ScienceOn
49	Cha, K.W., Lee, Y.J., Koh, H.J., Lee, B.M., Nam Y.M., and Paek, N.C. (2002). Isolation, characterization, and mapping of the stay green mutant in rice. Theor. Appl. Genet. 104, 526-532. DOI
50	Clerkx, E.J., Vries, H.B., Ruys, G.J., Groot, S.P., and Koornneef, M. (2003). Characterization of green seed, an enhancer of abi3-1 in Arabidopsis that affects seed longevity. Plant Physiol. 132, 1077-1084. DOI ScienceOn
51	Delmas, F., Sankaranarayanan, S., Deb, S., Widdup, E., Bournonville, C., Bollier, N., Northey, J.G.B., McCourt, P., and Samuel, M.A. (2013). ABI3 controls embryo degreening through Mendel's I locus. Proc. Natl. Acad. Sci. USA 110, e3888-e3894. DOI ScienceOn
52	Fang, C., Li, C., Li, W., Wang, Z., Zhou, Z., Shen, Y., Wu, M., Wu, Y., Li, G., Kong, L.A., et al. (2014). Concerted evolution of D1 and D2 to regulate chlorophyll degradation in soybean. Plant J. 77, 700-712. DOI ScienceOn
53	Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., et al. (2009). Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123-2132. DOI ScienceOn
54	Forsberg, J., Strom, J., Kieselbach, H., Larsson, K., Alexciev, A., Engstrom, A., and Akerlund, H.E. (2005). Protease activities in the chloroplast capable of cleaving an LHCII N-terminal peptide. Physiol. Plant. 123, 21-29. DOI ScienceOn
55	Fraser, P.D., Truesdale, M.R., Bird, C.R., Schuch, W., and Bramley, P.M. (1994). Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol. 105, 405-413. DOI
56	Fraser, P.D., and Bramley, P.M. (2004). The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res. 43, 228-265 DOI ScienceOn
57	Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F., and Goodman, H.M. (1992). Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4, 1251-1261. DOI ScienceOn
58	Gray, J., Close, P.S., Briggs, S.P., and Johal, G.S. (1997). A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89, 25-31. DOI ScienceOn
59	Gray, J., Janick-Buckner, D., Buckner, B., Close, P.S., and Johal, G.S. (2002). Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 130, 1894-1907. DOI ScienceOn
60	Guiamet, J.J., Schwartz, E., Pichersky, E., and Nooden, L.D. (1991). Characterization of cytoplasmic and nuclear mutations affecting chlorophyll and chlorophyll-binding proteins during senescence in soybean. Plant Physiol. 96, 227-231. DOI ScienceOn

Reference

	Yanfei Liu. (2017) Frontiers in Plant Science Expression Differences of Pigment Structural Genes and Transcription Factors Explain Flesh Coloration in Three Contrasting Kiwifruit Cultivars / 8
1	Chihiro Oda-Yamamizo. (2016) Scientific Reports The NAC transcription factor ANAC046 is a positive regulator of chlorophyll degradation and senescence in Arabidopsis leaves / 6 (1)
3	X. Wang. (2017) Biologia Plantarum Soybean NAC gene family: sequence analysis and expression under low nitrogen supply / 61 (3) , 473
7	Mostafa Abdelrahman. (2017) Plant Cell Reports The “STAY-GREEN” trait and phytohormone signaling networks in plants under heat stress / 36 (7) , 1009
3	Qingjun Xie. (2016) Journal of Genetics and Genomics Involvement of a Putative Bipartite Transit Peptide in Targeting Rice Pheophorbide a Oxygenase into Chloroplasts for Chlorophyll Degradation during Leaf Senescence / 43 (3) , 145
12	Rui-Heng Wang. (2016) PLOS ONE Transcriptome Analysis Provides a Preliminary Regulation Route of the Ethylene Signal Transduction Component, SlEIN2, during Tomato Ripening / 11 (12) , e0168287
4	Shuya Shi. (2016) Acta Physiologiae Plantarum GmSGR1, a stay-green gene in soybean (Glycine max L.), plays an important role in regulating early leaf-yellowing phenotype and plant productivity under nitrogen deprivation / 38 (4)
1	Yasuhito Sakuraba. (2016) Plant Cell Reports Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription / 35 (1) , 155
1-2	Guangwen Lu. (2017) Plant Molecular Biology Overexpression of OsGATA12 regulates chlorophyll content, delays plant senescence and improves rice yield under high density planting / 94 (1-2) , 215
1	Ranjith Kumar Manoharan. (2017) Hereditas Molecular breeding of a novel orange-brown tomato fruit with enhanced beta-carotene and chlorophyll accumulation / 154 (1)
9	Galina Smolikova. (2017) International Journal of Molecular Sciences Genetic and Hormonal Regulation of Chlorophyll Degradation during Maturation of Seeds with Green Embryos / 18 (9) , 1993
10	(2015) Molecules and cells Rice 7-Hydroxymethyl Chlorophyll a Reductase Is Involved in the Promotion of Chlorophyll Degradation and Modulates Cell Death Signaling / 40 (10) , 773
3	(2018) Theoretical and Applied Genetics Genetic dissection of early-season cold tolerance in sorghum: genome-wide association studies for seedling emergence and survival under field and controlled environment conditions / 131 (3) , 581
1664-462X	(2018) Frontiers in Plant Science New Urea Derivatives Are Effective Anti-senescence Compounds Acting Most Likely via a Cytokinin-Independent Mechanism / 9 (1664-462X)
0028646X	(2019) New Phytologist ) R2R3-MYB transcription factor modulates chlorophyll and carotenoid accumulation / (0028646X)
0028646X	(2018) New Phytologist gene provides durable, broad-spectrum disease resistances for over 50 years of US cucumber production / (0028646X)
7	(2018) Theoretical and Applied Genetics STAYGREEN (CsSGR) is a candidate for the anthracnose (Colletotrichum orbiculare) resistance locus cla in Gy14 cucumber / 131 (7) , 1577
1	(2018) BMC Plant Biology Overexpression of the protein disulfide isomerase AtCYO1 in chloroplasts slows dark-induced senescence in Arabidopsis / 18 (1)
1664-462X	(2018) Frontiers in Plant Science Large-Scale Investigation of Soybean Gene Functions by Overexpressing a Full-Length Soybean cDNA Library in Arabidopsis / 9 (1664-462X)
09607412	(2019) The Plant Journal / (09607412)
None	(2015) Scientific reports Regulation of ethylene-responsive <I>SlWRKY</I> s involved in color change during tomato fruit ripening / 7 (None) , 16674
6	(2015) International journal of molecular sciences Transcriptome Profile of the Variegated <I>Ficus microcarpa</I> c.v. Milky Stripe Fig Leaf / 20 (6) , 1338
7	(2019) Plant cell reports Differentiation of chromoplasts and other plastids in plants / 38 (7) , 803
5	(2020) Functional plant biology : FPB Comparative analysis of the plastid conversion, photochemical activity and chlorophyll degradation in developing embryos of green-seeded and yellow-seeded pea (Pisum sativum) cultivars / 47 (5) , 409
None	(2015) Food chemistry Effects of 1-methylcyclopropene (1-MCP) on the expression of genes involved in the chlorophyll degradation pathway of apple fruit during storage / 308 (None) , 125707
4	(2015) Plants NH <SUB>4</SUB> <SUP>+</SUP> Toxicity, Which Is Mainly Determined by the High NH <SUB>4</SUB> <SUP>+</SUP> /K <SUP>+</SUP> Ratio, Is Alleviated by CIPK23 in <I>Arabidopsis</I> / 9 (4) , 501
7	(2015) Agronomy Deciphering the Role of Stay-Green Trait to Mitigate Terminal Heat Stress in Bread Wheat / 10 (7) , 1001
5	(2015) The journal of horticultural science & biotechnology Transcriptomic investigation of the basis of Corona and petal colour in Chinese narcissus / 95 (5) , 565
7	(2021) International journal of molecular sciences Light-Mediated Regulation of Leaf Senescence / 22 (7) , 3291
9	(2021) International journal of molecular sciences Current Understanding of Leaf Senescence in Rice / 22 (9) , 4515
7	(2015) Journal of biomolecular structure & dynamics Comprehensive study of the genes involved in chlorophyll synthesis and degradation pathways in some monocot and dicot plant species / 39 (7) , 2387
11	(2021) International journal of molecular sciences Comparative Transcriptome-Based Mining of Senescence-Related MADS, NAC, and WRKY Transcription Factors in the Rapid-Senescence Line DLS-91 of Brassica rapa / 22 (11) , 6017
2	(2015) New Zealand journal of crop and horticultural science Transcriptome analysis reveals the roles of chlorophyll <I>a</I>/<I>b</I>-binding proteins (CABs) and stay-green (SGR) in chlorophyll degradation during fruit development in kiwifruit / 49 (2) , 106
None	(2015) Scientia horticulturae Comprehensive insight into the chlorophyll degradation mechanism of postharvest broccoli heads under elevated O<SUB>2</SUB> controlled atmosphere / 288 (None) , 110395
None	(2015) Scientia horticulturae STAY-GREEN and light-harvesting complex II chlorophyll a/b binding protein are involved in albinism of a novel albino tea germplasm ‘Huabai 1’ / 293 (None) , 110653