Research Progress on the Mechanisms of Leaf Color Regulation and Related Genes in Rice

doi:10.11983/CBB23055

Abstract

Abstract: Photosynthesis of plants depends on the green leaves, and the most intuitive feature of leaf growth and development is its color. At present, more than 200 genes related to rice leaf color have been cloned. The regulatory mechanisms of rice leaf color are complex and diverse, which involve multiple regulatory pathways, including biosynthesis and degradation of photosynthetic pigments, pathway of nucleus-plastid signaling, and heme synthesis. In addition, external environment such as temperature and light intensity can also affect the color changes of rice leaves. Here we reviewed the molecular pathways of rice leaf color, environmental factors and leaf color related genes, as well as the genetic regulatory mechanisms of rice leaf color was revealed, which will provide theoretical basis for rice high photosynthetic breeding and application, and future research in addressing some scientific problems in this field.

Key words: rice, leaf color, regulatory mechanism

Dai Ruohui, Qian Xinyu, Sun Jinglei, Lu Tao, Jia Qiwei, Lu Tianqi, Lu Mei, Rao Yuchun. Research Progress on the Mechanisms of Leaf Color Regulation and Related Genes in Rice[J]. Chinese Bulletin of Botany, 2023, 58(5): 799-812.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB23055

https://www.chinbullbotany.com/EN/Y2023/V58/I5/799

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References 106

[1]	白霞 (2017). 水稻多分枝和淡黄叶突变体buy1的分离及基因功能分析. 硕士论文. 杭州: 杭州师范大学. pp. 36.
[2]	杜逸凡, 刘芬, 刘坤, 吴旺嫔, 王悦, 陈光辉 (2019). 节水灌溉下南方双季稻区主栽机插水稻品种的光合特性和产量. 热带作物学报 40, 2047-2053.
[3]	樊宝莲, 王晓云 (2021). 转录因子调控植物类胡萝卜素合成途径的研究进展. 分子植物育种 19, 4401-4408.
[4]	费小红, 安保光, 赵宝华, 李阳生 (2009). 类胡萝卜素参与水稻抗氧化胁迫的研究进展. 现代农业科学 16, 22-23.
[5]	姜卫兵, 庄猛, 韩浩章, 戴美松, 花国平 (2005). 彩叶植物呈色机理及光合特性研究进展. 园艺学报 32, 352-358.
[6]	李蒙 (2019). 水稻氮利用相关基因OsDNU1的定位克隆与功能初步研究. 硕士论文. 雅安: 四川农业大学. pp. 38-39.
[7]	李逸心, 朱桂才 (2022). 植物叶色变异机理的研究进展. 农业与技术 42, 1-3. DOI
[8]	刘国民, 高必军, 文绍山, 焦峻 (2010). 具有黄绿叶标记的香型籼稻不育系选育研究. 中国农业科学 43, 855-861.
[9]	刘珊珊, 符辰建, 秦鹏, 黎琛子, 胡小淳, 符星学, 吴挺飞, 杨远柱 (2021). 绿色优质高产广适超级杂交稻隆两优1308的选育. 农业科技通讯 (5), 279-283.
[10]	刘艳霞, 林冬枝, 董彦君 (2015). 水稻温敏感叶色突变体研究进展. 中国水稻科学 29, 439-446. DOI
[11]	罗治靖, 沈卫平, 陈明姣, 梁婉琪, 陆建忠, 张建中, 刘康, 张大兵, 袁政 (2013). 淡黄叶优质粳稻不育系金汇A的选育. 杂交水稻 28(3), 12-14.
[12]	马玉巧 (2020). OsLIL3调控水稻叶绿素合成的分子机制. 硕士论文. 扬州: 扬州大学. pp. 16-17.
[13]	孟祥州, 严菊, 邢宏堃, 王功伟 (2015). 水稻NOL (NYC1- like)基因序列多样性、单倍型效应以及表达谱分析. 分子植物育种 13, 491-496.
[14]	钱前, 朱旭东, 曾大力, 张小惠, 严学强, 熊振民 (1996). 细胞质基因控制的新特异材料白绿苗的研究. 作物品种资源 (4), 13-14.
[15]	秦丹丹, 李梅芳, 许甫超, 徐晴, 葛双桃, 董静 (2019). 大麦黄绿叶色突变体ygl的农艺性状及其调控基因初步定位. 麦类作物学报 39, 653-658.
[16]	孙旺旺 (2018). 金叶金钟花叶片色素含量年变化及解剖结构特征. 硕士论文. 秦皇岛: 河北科技师范学院. pp. 5.
[17]	王中豪, 贺彦, 张晓波, 徐霞, 吴建利, 施勇烽 (2021). 水稻白化转绿和穗顶端退化突变体vpa1的遗传分析和基因定位. 中国水稻科学 35, 19-26. DOI
[18]	吴殿星, 舒庆尧, 夏英武, 夏建峰 (1999). 水稻转绿型白化突变系W²⁵返白复绿过程中叶片的生理变化. 浙江农业大学学报 (1), 3-6.
[19]	叶琳珊 (2018). GTP结合蛋白EMB2738和硫氧还蛋白AtECB1调控叶绿体发育的机理研究. 博士论文. 上海: 上海师范大学. pp. 15.
[20]	赵娟 (2014). 水稻编码类胡萝卜素异构酶基因ZEBRA LEAF 2的鉴定与克隆. 硕士论文. 杭州: 中国计量学院. pp. 33-35.
[21]	赵绍路, 刘凯, 宛柏杰, 朱静雯, 刘艳艳, 唐红生, 严国红, 孙明法 (2018). 水稻叶色突变研究进展. 大麦与谷类科学 35 (6), 1-6.
[22]	周琳, 梁轩铭, 赵磊 (2022). 天然类胡萝卜素的生物合成研究进展. 生物技术通报 38(7), 119-127. DOI
[23]	Awan MA, Konzak CF, Rutger JN, Nilan RA (1980). Mutagenic effects of sodium azide in rice. Crop Sci 20, 663-668. DOI URL
[24]	Cao PH, Ren YK, Liu X, Zhang TY, Zhang P, Xiao LJ, Zhang FL, Liu SJ, Jiang L, Wan JM (2019). Purine nucleotide biosynthetic gene GARS controls early chloroplast development in rice (Oryza sativa L.). Plant Cell Rep 38, 183-194. DOI
[25]	Chai CL, Fang J, Liu Y, Tong HN, Gong YQ, Wang YQ, Liu M, Wang YP, Qian Q, Cheng ZK, Chu CC (2011). ZEBRA2, encoding a carotenoid isomerase, is involved in photoprotection in rice. Plant Mol Biol 75, 211-221. DOI PMID
[26]	Chen H, Cheng ZJ, Ma XD, Wu H, Liu YL, Zhou KN, Chen YL, Ma WW, Bi JC, Zhang X, Guo XP, Wang JL, Lei CL, Wu FQ, Lin QB, Liu YQ, Liu LL, Jiang L (2013). A knockdown mutation of YELLOW-GREEN LEAF 2 blocks chlorophyll biosynthesis in rice. Plant Cell Rep 32, 1855-1867. DOI URL
[27]	Chen NG, Wang PR, Li CM, Wang Q, Pan JH, Xiao FL, Wang Y, Zhang K, Li CX, Yang B, Sun CH, Deng XJ (2018). A single nucleotide mutation of the IspE gene participating in the MEP pathway for isoprenoid biosynthesis causes a green-revertible yellow leaf phenotype in rice. Plant Cell Physiol 59, 1905-1917. DOI URL
[28]	Chen PF, Liu X, Gu CH, Zhong PY, Song N, Li MB, Dai ZQ, Fang XQ, Liu ZM, Zhang JF, Tang RK, Fan SW, Lin XF (2022a). A plant-derived natural photosynthetic system for improving cell anabolism. Nature 612, 546-554. DOI
[29]	Chen SJ, Zeng XH, Li YQ, Qiu SJ, Peng XQ, Xie XJ, Liu YJ, Liao CC, Tang XY, Wu JX (2022b). The nuclear- encoded plastid ribosomal protein L18s are essential for plant development. Front Plant Sci 13, 949897. DOI URL
[30]	Demarsy E, Courtois F, Azevedo J, Buhot L, Lerbs-Mache S (2006). Building up of the plastid transcriptional machinery during germination and early plant development. Plant Physiol 142, 993-1003. PMID
[31]	Du YX, Mo WP, Ma TT, Tang WJ, Tian LJ, Lin RC (2021). A pentatricopeptide repeat protein DUA1 interacts with sigma factor 1 to regulate chloroplast gene expression in rice. Photosynth Res 147, 131-143. DOI
[32]	Fang J, Chai CL, Qian Q, Li CL, Tang JY, Sun L, Huang ZJ, Guo XL, Sun CH, Liu M, Zhang Y, Lu QT, Wang YQ, Lu CM, Han B, Chen F, Cheng ZK, Chu CC (2008). Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo- oxidation in rice. Plant J 54, 177-189. DOI URL
[33]	Fang YX, Hou LL, Zhang XQ, Pan JJ, Ren DY, Zeng DL, Guo LB, Qian Q, Hu J, Xue DW (2019). Disruption of ζ-carotene desaturase protein ALE1 leads to chloroplast developmental defects and seedling lethality. J Agric Food Chem 67, 11607-11615. DOI URL
[34]	Gao TM, Wei SL, Chen J, Wu Y, Li F, Wei LB, Li C, Zeng YJ, Tian Y, Wang DY, Zhang HY (2020). Cytological, genetic, and proteomic analysis of a sesame (Sesamum indicum L.) mutant Siyl-1 with yellow-green leaf color. Ge- nes Genom 42, 25-39.
[35]	Gong XD, Jiang Q, Xu JL, Zhang JH, Teng S, Lin DZ, Dong YJ (2013). Disruption of the rice plastid ribosomal protein s20 leads to chloroplast developmental defects and seedling lethality. G3(Bethesda) 3, 1769-1777. DOI URL
[36]	Gong XD, Su QQ, Lin DZ, Jiang Q, Xu JL, Zhang JH, Teng S, Dong YJ (2014). The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress. J Integr Plant Biol 56, 400-410. DOI URL
[37]	Gothandam KM, Kim ES, Cho H, Chung YY (2005). OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58, 421-433. PMID
[38]	Inagaki N, Kinoshita K, Kagawa T, Tanaka A, Ueno O, Shimada H, Takano M (2015). Phytochrome B mediates the regulation of chlorophyll biosynthesis through transcriptional regulation of ChlH and GUN4 in rice seedlings. PLoS One 10, e0135408.
[39]	Jung KH, Hur JH, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An G (2003). Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44, 463-472. DOI URL
[40]	Kim SH, Kwon CT, Song G, Koh HJ, An G, Paek NC (2018). The rice zebra3 (z3) mutation disrupts citrate distribution and produces transverse dark-green/green variegation in mature leaves. Rice 11, 1. DOI URL
[41]	Kong WY, Yu XW, Chen HY, Liu LL, Xiao YJ, Wang YL, Wang CL, Lin Y, Yu Y, Wang CM, Jiang L, Zhai HQ, Zhao ZG, Wan JM (2016). The catalytic subunit of magnesium-protoporphyrin IX monomethyl ester cyclase forms a chloroplast complex to regulate chlorophyll biosynthesis in rice. Plant Mol Biol 92, 177-191. DOI PMID
[42]	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 COLORING 1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19, 1362-1375. DOI URL
[43]	Kusumi K, Komori H, Satoh H, Iba K (2000). Characterization of a zebra mutant of rice with increased susceptibility to light stress. Plant Cell Physiol 41, 158-164. PMID
[44]	Kusumi K, Sakata C, Nakamura T, Kawasaki S, Yoshimura A, Iba K (2011). A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress conditions. Plant J 68, 1039-1050. DOI URL
[45]	Laloi C, Przybyla D, Apel K (2006). A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J Exp Bot 57, 1719-1724. DOI URL
[46]	Lee J, Jang S, Ryu S, Lee S, Park J, Lee S, An G, Park SK (2019). Mutation of plastid ribosomal protein L13 results in an albino seedling-lethal phenotype in rice. Plant Breed Biotech 7, 395-404. DOI URL
[47]	Lee KP, Kim C, Landgraf F, Apel K (2007). EXECUTER1- and EXECUTER2-dependent transfer of stress- related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104, 10270-10275. DOI URL
[48]	Lee S, Kim JH, Yoo ES, Lee CH, Hirochika H, An G (2005). Differential regulation of chlorophyll a oxygenase genes in rice. Plant Mol Biol 57, 805-818. PMID
[49]	Legen J, Ruf S, Kroop X, Wang GW, Barkan A, Bock R, Schmitz-Linneweber C (2018). Stabilization and translation of synthetic operon-derived mRNAs in chloroplasts by sequences representing PPR protein-binding sites. Plant J 94, 8-21. DOI URL
[50]	Li CM, Liu X, Pan JH, Guo J, Wang Q, Chen CP, Li N, Zhang K, Yang B, Sun CH, Deng XJ, Wang PR (2019). A lil3/chlp double mutant with exclusive accumulation of geranylgeranyl chlorophyll displays a lethal phenotype in rice. BMC Plant Biol 19, 456. DOI
[51]	Li HC, Ji GB, Wang Y, Qian Q, Xu JC, Sodmergen, Liu GZ, Zhao XF, Chen MS, Zhai WX, Li DY, Zhu LH (2018). WHITE PANICLE 3, a novel nucleus-encoded mitochondrial protein, is essential for proper development and maintenance of chloroplasts and mitochondria in rice. Front Plant Sci 9, 762.
[52]	Li JQ, Wang YH, Chai JT, Wang LH, Wang CM, Long WH, Wang D, Wang YL, Zheng M, Peng C, Niu M, Wan JM (2013). grc1) is required for the biosynthesis of chlorophyll and the early development of chloroplasts in rice. J Plant Biol 56, 326-335. DOI URL
[53]	Lin D, Jiang Q, Zheng K, Chen S, Zhou H, Gong X, Xu J, Teng S, Dong Y (2015a). Mutation of the rice ASL2 gene encoding plastid ribosomal protein L21 causes chloroplast developmental defects and seedling death. Plant Biol 17, 599-607. DOI URL
[54]	Lin DZ, Gong XD, Jiang Q, Zheng KL, Zhou H, Xu JL, Teng S, Dong YJ (2015b). The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth. Rice 8, 17. DOI URL
[55]	Lin DZ, Jiang Q, Ma XJ, Zheng KL, Gong XD, Teng S, Xu JL, Dong YJ (2018). Rice TSV3 encoding obg-like GTPase protein is essential for chloroplast development during the early leaf stage under cold stress. G3 (Bethesda) 8, 253-263. DOI URL
[56]	Liu HJ, Li QZ, Yang F, Zhu FY, Sun Y, Tao YZ, Lo C (2016). Differential regulation of protochlorophyllide oxidoreductase abundances by VIRESCENT 5A (OsV_5A) and VIRESCENT 5B (OsV_5B) in rice seedlings. Plant Cell Physiol 57, 2392-2402. PMID
[57]	Liu LH, Ren MM, Peng P, Chun Y, Li L, Zhao JF, Fang JJ, Peng LX, Yan JJ, Chu JF, Wang YQ, Yuan SJ, Li XY (2021a). MIT1, encoding a 15-cis-ζ-carotene isomerase, regulates tiller number and stature in rice. J Genet Genomics 48, 88-91. DOI URL
[58]	Liu LL, You J, Zhu Z, Chen KY, Hu MM, Gu H, Liu ZW, Wang ZY, Wang YH, Liu SJ, Chen LM, Liu X, Tian YL, Zhou SR, Jiang L, Wan JM (2020). WHITE STRIPE LEAF 8, encoding a deoxyribonucleoside kinase, is involved in chloroplast development in rice. Plant Cell Rep 39, 19-33. DOI PMID
[59]	Liu WZ, Fu YP, Hu GC, Si HM, Zhu L, Wu C, Sun ZX (2007). Identification and fine mapping of a thermo-sensitive chlorophyll deficient mutant in rice (Oryza sativa L.). Planta 226, 785-795. DOI URL
[60]	Liu XY, Zhang XC, Cao RJ, Jiao GA, Hu SK, Shao GN, Sheng ZH, Xie LH, Tang SQ, Wei XJ, Hu PS (2021b). CDE4 encodes a pentatricopeptide repeat protein involved in chloroplast RNA splicing and affects chloroplast development under low-temperature conditions in rice. J Integr Plant Biol 63, 1724-1739. DOI URL
[61]	Lv J, Shang LG, Chen Y, Han Y, Yang XY, Xie SZ, Bai WQ, Hu MY, Wu H, Lei KR, Yang Y, Ge SZ, Trinh HP, Zhang Y, Guo LB, Wang ZW (2020). OsSLC1 encodes a pentatricopeptide repeat protein essential for early chloroplast development and seedling survival. Rice 13, 25. DOI
[62]	Lv YS, Shao GN, Qiu JH, Jiao GA, Sheng ZH, Xie LH, Wu YW, Tang SQ, Wei XJ, Hu PS (2017). White Leaf and Panicle 2, encoding a PEP-associated protein, is required for chloroplast biogenesis under heat stress in rice. J Exp Bot 68, 5147-5160. DOI PMID
[63]	Mahawar L, Shekhawat GS (2018). Haem oxygenase: a functionally diverse enzyme of photosynthetic organisms and its role in phytochrome chromophore biosynthesis, cellular signaling and defence mechanisms. Plant Cell En- viron 41, 483-500.
[64]	Matringe M, Camadro JM, Block MA, Joyard J, Scalla R, Labbe P, Douce R (1992). Localization within chloroplasts of protoporphyrinogen oxidase, the target enzyme for diphenylether-like herbicides. J Biol Chem 267, 4646-4651. PMID
[65]	Mei JS, Li FF, Liu XR, Hu GC, Fu YP, Liu WZ (2017). Newly identified CSP41b gene localized in chloroplasts affects leaf color in rice. Plant Sci 256, 39-45. DOI URL
[66]	Park H, Kreunen SS, Cuttriss AJ, Dellapenna D, Pogson BJ (2002). Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14, 321-332. DOI PMID
[67]	Pesaresi P, Schneider A, Kleine T, Leister D (2007). Interorganellar communication. Curr Opin Plant Biol 10, 600-606. PMID
[68]	Qiu ZN, Chen DD, He L, Zhang S, Yang ZN, Zhang Y, Wang ZW, Ren DY, Qian Q, Guo LB, Zhu L (2018a). The rice white green leaf 2 gene causes defects in chloroplast development and affects the plastid ribosomal protein S9. Rice 11, 39. DOI
[69]	Qiu ZN, Kang SJ, He L, Zhao J, Zhang S, Hu J, Zeng DL, Zhang GH, Dong GJ, Gao ZY, Ren DY, Chen G, Guo LB, Qian Q, Zhu L (2018b). The newly identified heat- stress sensitive albino 1 gene affects chloroplast development in rice. Plant Sci 267, 168-179. DOI URL
[70]	Rong H, Tang YY, Zhang H, Wu PZ, Chen YP, Li MR, Wu GJ, Jiang HW (2013). The Stay-Green Rice Like (SGRL) gene regulates chlorophyll degradation in rice. J Plant Physiol 170, 1367-1373.
[71]	Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andrèss CB, Kessler F, Hörtensteiner 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, 507-518. DOI URL
[72]	Scheumann V, Schoch S, Rüdiger W (1998). Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273, 35102-35108. DOI PMID
[73]	Song J, Wei XJ, Shao GN, Sheng ZH, Chen DB, Liu CL, Jiao GA, Xie LH, Tang SQ, Hu PS (2014). The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions. Plant Mol Biol 84, 301-314.
[74]	Sugimoto H, Kusumi K, Noguchi K, Yano M, Yoshimura A, Iba K (2007). The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. Plant J 52, 512-527. DOI PMID
[75]	Sugimoto H, Kusumi K, Tozawa Y, Yazaki J, Kishimoto N, Kikuchi S, Iba K (2004). The virescent-2 mutation inhibits translation of plastid transcripts for the plastid genetic system at an early stage of chloroplast differentiation. Plant Cell Physiol 45, 985-996. DOI PMID
[76]	Sun YL, Tian YL, Cheng SH, Wang YL, Hao YY, Zhu JP, Zhu XP, Zhang YY, Yu MZ, Lei J, Bao XH, Wu HM, Wang YH, Wan JM (2019). WSL6 encoding an Era-type GTP-binding protein is essential for chloroplast development in rice. Plant Mol Biol 100, 635-645. DOI
[77]	Tanaka R, Kobayashi K, Masuda T (2011). Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9, e0145.
[78]	Tang JP, Zhang WW, Wen K, Chen GM, Sun J, Tian YL, Tang WJ, Yu J, An HZ, Wu TT, Kong F, Terzaghi W, Wang CM, Wan JM (2017). OsPPR6, a pentatricopeptide repeat protein involved in editing and splicing chloroplast RNA, is required for chloroplast biogenesis in rice. Plant Mol Biol 95, 345-357. DOI PMID
[79]	Terry MJ, Kendrick RE (1999). Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore- deficient aurea and yellow-green-2 mutants of tomato. Plant Physiol 119, 143-152. PMID
[80]	von Wettstein D, Gough S, Kannangara CG (1995). Chlorophyll biosynthesis. Plant Cell 7, 1039-1057. DOI URL
[81]	Wang PR, Gao JX, Wan CM, Zhang FT, Xu ZJ, Huang XQ, Sun XQ, Deng XJ (2010). Divinyl chlorophyll(ide) a can be converted to monovinyl chlorophyll(ide) a by a divinyl reductase in rice. Plant Physiol 153, 994-1003. DOI URL
[82]	Wang PR, Wan CM, Xu ZJ, Wang PY, Wang WM, Sun CH, Ma XZ, Xiao YH, Zhu JQ, Gao XL, Deng XJ (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, 521-534. DOI PMID
[83]	Wang WJ, Zheng KL, Gong XD, Xu JL, Huang JR, Lin DZ, Dong YJ (2017a). The rice TCD11 encoding plastid ribosomal protein S6 is essential for chloroplast development at low temperature. Plant Sci 259, 1-11. DOI URL
[84]	Wang Y, Ren YL, Zhou KN, Liu LL, Wang JL, Xu Y, Zhang H, Zhang L, Feng ZM, Wang LW, Ma WW, Wang YL, Guo XP, Zhang X, Lei CL, Cheng ZJ, Wan JM (2017b). WHITE STRIPE LEAF 4 encodes a novel P-type PPR protein required for chloroplast biogenesis during early leaf development. Front Plant Sci 8, 1116. DOI URL
[85]	Wang YF, Zhang JH, Shi XL, Peng Y, Li P, Lin DZ, Dong YJ, Teng S (2016a). Temperature-sensitive albino gene TCD5, encoding a monooxygenase, affects chloroplast development at low temperatures. J Exp Bot 67, 5187-5202. DOI URL
[86]	Wang YL, Wang CM, Zheng M, Lyu J, Xu Y, Li XH, Niu M, Long WH, Wang D, Wang HY, Terzaghi W, Wang YH, Wan JM (2016b). WHITE PANICLE 1, a val-tRNA synthetase regulating chloroplast ribosome biogenesis in rice, is essential for early chloroplast development. Plant Physiol 170, 2110-2123. DOI URL
[87]	Wang YL, Wang YH, Ren YL, Duan EC, Zhu XP, Hao YY, Zhu JP, Chen RB, Lei J, Teng X, Zhang YY, Wang D, Zhang X, Guo XP, Jiang L, Liu SJ, Tian YL, Liu X, Chen LM, Wang HY, Wan JM (2021). White panicle 2 encoding thioredoxin z, regulates plastid RNA editing by interacting with multiple organellar RNA editing factors in rice. New Phytol 229, 2693-2706. DOI PMID
[88]	Woodson J, Perez-Ruiz J, Chory J (2011). Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr Biol 21, 897-903. DOI PMID
[89]	Wu LL, Wu J, Liu YX, Gong XD, Xu JL, Lin DZ, Dong YJ (2016). The rice pentatricopeptide repeat gene TCD10 is needed for chloroplast development under cold stress. Rice 9, 67. DOI URL
[90]	Wu ZM, Zhang X, He B, Diao LP, Sheng SL, Wang JL, Guo XP, Su N, Wang LF, Jiang L, Wang CM, Zhai HQ, Wan JM (2007). A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiol 145, 29-40. DOI PMID
[91]	Yamaguchi K, Subramanian AR (2000). The plastid ribosomal proteins: identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275, 28466-28482. DOI PMID
[92]	Yamatani H, Kohzuma K, Nakano M, Takami T, Kato Y, Hayashi Y, Monden Y, Okumoto Y, Abe T, Kumamaru T, Tanaka A, Sakamoto W, Kusaba M (2018). Impairment of Lhca4, a subunit of LHCI, causes high accumulation of chlorophyll and the stay-green phenotype in rice. J Exp Bot 69, 1027-1035. DOI PMID
[93]	Yang YL, Xu J, Huang LC, Leng YJ, Dai LP, Rao YC, Chen L, Wang YQ, Tu ZJ, Hu J, Ren DY, Zhang GH, Zhu L, Guo LB, Qian Q, Zeng DL (2016). PGL, encoding chlorophyllide a oxygenase 1, impacts leaf senescence and indirectly affects grain yield and quality in rice. J Exp Bot 67, 1297-1310. DOI PMID
[94]	Yap A, Kindgren P, Francs-Small CCD, Kazama T, Tanz SK, Toriyama K, Small I (2015). AEF1/MPR25 is implicated in RNA editing of plastid atpF and mitochondrial nad5, and also promotes atpF splicing in Arabidopsis and rice. Plant J 81, 661-669. DOI URL
[95]	Zeng ZQ, Lin TZ, Zhao JY, Zheng TH, Xu LF, Wang YH, Liu LL, Jiang L, Chen SH, Wan JM (2020). OsHemA gene, encoding glutamyl-tRNA reductase (GluTR) is essential for chlorophyll biosynthesis in rice (Oryza sativa). J Integr Agric 19, 612-623. DOI
[96]	Zhang H, Liu LL, Cai MH, Zhu SS, Zhao JY, Zheng TH, Xu XY, Zeng ZQ, Niu J, Jiang L, Chen SH, Wan JM (2015). A point mutation of magnesium chelatase OsCHLI gene dampens the interaction between CHLI and CHLD subunits in rice. Plant Mol Biol Rep 33, 1975-1987. DOI URL
[97]	Zhang HT, Li JJ, Yoo JH, Yoo SC, Cho SH, Koh HJ, Seo HS, Paek NC (2006). Rice chlorina-1 and chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62, 325-337. DOI URL
[98]	Zhang Q, Shen L, Wang ZW, Hu GL, Ren DY, Hu J, Zhu L, Gao ZY, Zhang GH, Guo LB, Zeng DL, Qian Q (2019). OsCAF1, a CRM domain containing protein, influences chloroplast development. Int J Mol Sci 20, 4386. DOI URL
[99]	Zhang T, Feng P, Li YF, Yu P, Yu GL, Sang XC, Ling YH, Zeng XQ, Li YD, Huang JY, Zhang TQ, Zhao FM, Wang N, Zhang CW, Yang ZL, Wu RH, He GH (2018). VIRESCENT-ALBINO LEAF 1 regulates leaf colour development and cell division in rice. J Exp Bot 69, 4791-4804. DOI PMID
[100]	Zhang ZG, Cui XA, Wang YW, Wu JX, Gu XF, Lu TG (2017). The RNA editing factor WSP1 is essential for chloroplast development in rice. Mol Plant 10, 86-98. DOI URL
[101]	Zhao J, Qiu ZN, Ruan BP, Kang SJ, He L, Zhang S, Dong GJ, Hu J, Zeng DL, Zhang GH, Gao ZY, Ren DY, Hu XM, Chen G, Guo LB, Qian Q, Zhu L (2015). Functional inactivation of putative photosynthetic electron acceptor ferredoxin C2 (FdC2) induces delayed heading date and decreased photosynthetic rate in rice. PLoS One 10, e014-3361.
[102]	Zhao XB, Huang JY, Chory J (2019). GUN1 interacts with MORF2 to regulate plastid RNA editing during retrograde signaling. Proc Natl Acad Sci USA 116, 10162-10167. DOI URL
[103]	Zheng KL, Zhao J, Lin DZ, Chen JY, Xu JL, Zhou H, Teng S, Dong YJ (2016). The rice TCM5 gene encoding a novel deg protease protein is essential for chloroplast development under high temperatures. Rice 9, 13. DOI URL
[104]	Zhou SX, Sawicki A, Willows RD, Luo MZ (2012). C-terminal residues of Oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis. FEBS Lett 586, 205-210. DOI URL
[105]	Zhu XB, Ze M, Yin JJ, Chern M, Wang MR, Zhang X, Deng R, Li YZ, Liao HC, Wang L, Tu B, Song L, He M, Li SG, Wang WM, Chen XW, Wang J, Li WT (2020a). A phosphofructokinase B-type carbohydrate kinase family protein, PFKB1, is essential for chloroplast development at early seedling stage in rice. Plant Sci 290, 110295. DOI URL
[106]	Zhu XJ, Mou CL, Zhang FL, Huang YS, Yang CY, Ji JL, Liu X, Cao PH, Nguyen T, Lan J, Zhou CL, Liu SJ, Jiang L, Wan JM (2020b). WSL9 encodes an HNH endonuclease domain-containing protein that is essential for early chloroplast development in rice. Rice 13, 45. DOI

调控途径	基因	表型	染色体定位	基因功能	参考文献
叶绿素	LYL1	黄化	2	编码叶绿体信号识别颗粒	Li et al., 2019
合成	CHLD	黄化	3	镁离子螯合酶D亚基	Zhang et al., 2015
	CHLI	黄绿叶	3	镁离子螯合酶I亚基	Zhang et al., 2015
	CHLH	白化	3	镁离子螯合酶H亚基	Zhou et al., 2012
	HemA	淡绿	10	谷氨酰-tRNA还原酶基因	Zeng et al., 2020
	YLC2	黄叶	3	亚铁血红素加氧酶基因	Mahawar and Shekhawat, 2018
	FdC2	黄绿叶	3	编码铁氧还蛋白类似物, 调节电子转移和叶绿	Zhao et al., 2015
	FdC2	黄绿叶	3	素含量	Zhao et al., 2015
	PORA	黄化	4	原叶绿素酸酯氧化还原酶A基因	Liu et al., 2016
	PORB	淡绿	10	原叶绿素酸酯氧化还原酶B基因	Liu et al., 2016
	YGL1	黄绿叶	5	叶绿素合成酶基因	Liu et al., 2016
	YGL2	黄叶	6	编码血红素加氧酶	Chen et al., 2013
	CAO1	淡绿	10	叶绿素a加氧酶基因	Yang et al., 2015
	CAO2	敲除无差异	10	叶绿素a加氧酶基因	Yang et al., 2015
	YL1	黄绿叶	2	编码光诱导叶绿体蛋白	Wang et al., 2017b
	V5A	黄叶	9	与OsPORA和OsPORB互作, 调控叶绿素合成	Liu et al., 2016
叶绿素	NOL	永绿	3	叶绿素b还原酶基因	孟祥州等, 2015
降解	DVR	黄绿叶	3	编码联乙烯还原酶	Wang et al., 2013
	SGRL	持绿	4	参与叶绿素分解	Rong et al., 2013
	VAL1	白化转绿	8	嘌呤核苷酸生物合成酶基因	Zhang et al., 2018
	DYE1	持绿	8	编码捕光复合体I亚基	Yamatani et al., 2018
类胡萝	PDS	白化	3	编码ABA合成	Fang et al., 2019
卜素	IspE	黄化转绿	1	参与异戊二烯生物合成	Chen et al., 2018
合成	MIT1	持绿	12	编码胡萝卜素异构酶	Liu et al., 2021a
	ZEBRA2	斑马叶	11	类胡萝卜素异构酶基因	Chai et al., 2011
核-质信	WLP2	白叶和白穗	1	编码质体编码的RNA聚合酶相关蛋白	Lv et al., 2017
号转导	WSL	白条纹叶	1	编码PPR蛋白, 参与叶绿体RNA剪接	Wang et al., 2017b
相关	WSL4	温敏条纹	2	编码PPR蛋白, 参与叶绿体RNA剪接	Wang et al., 2017b
	WSL9	白叶条纹	3	编码含HNH核酸内切酶结构域的蛋白质	Zhu et al., 2020b
	CAF1	白化致死	1	编码叶绿体RNA剪接因子	Zhang et al., 2019
	SLA4	白化	7	编码PPR蛋白, 参与RNA剪接	Lv et al., 2020
	WSP1	白条纹叶和白穗	4	叶绿体基因RNA编辑因子, 编码MORF家族蛋白	Zhang et al., 2017
	PPR6	白化致死	5	编码PPR蛋白, 参与叶绿体RNA编辑与剪接	Tang et al., 2017
	DUA1	低温白化	9	编码PPR蛋白, 参与叶绿体RNA编辑	Yap et al., 2015
	Z3	斑马叶	3	编码柠檬酸转运蛋白	Kim et al., 2018
叶绿体	ASL1	白化致死	1	编码叶绿体核糖体蛋白	Song et al., 2014
发育相	ALS3	白化致死	1	编码叶绿体靶向的PPR蛋白, 含有10个串联	Lin et al., 2018
关	ALS3	白化致死	1	的PPR基序	Lin et al., 2018
	WP3	幼苗白条纹	1	编码靶向线粒体的蛋白质	Li et al., 2018
	WSL6	白条纹叶	5	编码GTP结合蛋白	Sun et al., 2019
	TSV3	温敏白化	3	编码GTP结合蛋白	Lin et al., 2018
	WSL8	白条纹叶	5	脱氧核糖核酸激酶基因	Liu et al., 2020
	V1	温敏白化转绿	3	编码叶绿体定位蛋白NUS1, 参与叶绿体RNA	Kusumi et al., 2011
	V1	温敏白化转绿	3	代谢调节	Kusumi et al., 2011
	V3	白化转绿	6	编码核糖核酸还原酶大亚基	Inagaki et al., 2015
	V4	低温白化	7	编码PPR蛋白	Lv et al., 2020
	TCD5	温敏白化	5	单加氧酶基因	Wang et al., 2016a
	GARS	白条纹叶	8	编码一种催化嘌呤核苷酸生物合成第2步的酶	Cao et al., 2018
	YGL8	黄叶	1	编码尿嘧啶核苷酸激酶	Kong et al., 2016
	Rey(k2)	黄化转绿	10	磷酸果糖激酶B型碳水化合物激酶基因	Zhu et al., 2020a

调控途径	基因	表型	染色体定位	基因功能	参考文献
叶绿素	LYL1	黄化	2	编码叶绿体信号识别颗粒	Li et al., 2019
合成	CHLD	黄化	3	镁离子螯合酶D亚基	Zhang et al., 2015
	CHLI	黄绿叶	3	镁离子螯合酶I亚基	Zhang et al., 2015
	CHLH	白化	3	镁离子螯合酶H亚基	Zhou et al., 2012
	HemA	淡绿	10	谷氨酰-tRNA还原酶基因	Zeng et al., 2020
	YLC2	黄叶	3	亚铁血红素加氧酶基因	Mahawar and Shekhawat, 2018
	FdC2	黄绿叶	3	编码铁氧还蛋白类似物, 调节电子转移和叶绿	Zhao et al., 2015
	FdC2	黄绿叶	3	素含量	Zhao et al., 2015
	PORA	黄化	4	原叶绿素酸酯氧化还原酶A基因	Liu et al., 2016
	PORB	淡绿	10	原叶绿素酸酯氧化还原酶B基因	Liu et al., 2016
	YGL1	黄绿叶	5	叶绿素合成酶基因	Liu et al., 2016
	YGL2	黄叶	6	编码血红素加氧酶	Chen et al., 2013
	CAO1	淡绿	10	叶绿素a加氧酶基因	Yang et al., 2015
	CAO2	敲除无差异	10	叶绿素a加氧酶基因	Yang et al., 2015
	YL1	黄绿叶	2	编码光诱导叶绿体蛋白	Wang et al., 2017b
	V5A	黄叶	9	与OsPORA和OsPORB互作, 调控叶绿素合成	Liu et al., 2016
叶绿素	NOL	永绿	3	叶绿素b还原酶基因	孟祥州等, 2015
降解	DVR	黄绿叶	3	编码联乙烯还原酶	Wang et al., 2013
	SGRL	持绿	4	参与叶绿素分解	Rong et al., 2013
	VAL1	白化转绿	8	嘌呤核苷酸生物合成酶基因	Zhang et al., 2018
	DYE1	持绿	8	编码捕光复合体I亚基	Yamatani et al., 2018
类胡萝	PDS	白化	3	编码ABA合成	Fang et al., 2019
卜素	IspE	黄化转绿	1	参与异戊二烯生物合成	Chen et al., 2018
合成	MIT1	持绿	12	编码胡萝卜素异构酶	Liu et al., 2021a
	ZEBRA2	斑马叶	11	类胡萝卜素异构酶基因	Chai et al., 2011
核-质信	WLP2	白叶和白穗	1	编码质体编码的RNA聚合酶相关蛋白	Lv et al., 2017
号转导	WSL	白条纹叶	1	编码PPR蛋白, 参与叶绿体RNA剪接	Wang et al., 2017b
相关	WSL4	温敏条纹	2	编码PPR蛋白, 参与叶绿体RNA剪接	Wang et al., 2017b
	WSL9	白叶条纹	3	编码含HNH核酸内切酶结构域的蛋白质	Zhu et al., 2020b
	CAF1	白化致死	1	编码叶绿体RNA剪接因子	Zhang et al., 2019
	SLA4	白化	7	编码PPR蛋白, 参与RNA剪接	Lv et al., 2020
	WSP1	白条纹叶和白穗	4	叶绿体基因RNA编辑因子, 编码MORF家族蛋白	Zhang et al., 2017
	PPR6	白化致死	5	编码PPR蛋白, 参与叶绿体RNA编辑与剪接	Tang et al., 2017
	DUA1	低温白化	9	编码PPR蛋白, 参与叶绿体RNA编辑	Yap et al., 2015
	Z3	斑马叶	3	编码柠檬酸转运蛋白	Kim et al., 2018
叶绿体	ASL1	白化致死	1	编码叶绿体核糖体蛋白	Song et al., 2014
发育相	ALS3	白化致死	1	编码叶绿体靶向的PPR蛋白, 含有10个串联	Lin et al., 2018
关	ALS3	白化致死	1	的PPR基序	Lin et al., 2018
	WP3	幼苗白条纹	1	编码靶向线粒体的蛋白质	Li et al., 2018
	WSL6	白条纹叶	5	编码GTP结合蛋白	Sun et al., 2019
	TSV3	温敏白化	3	编码GTP结合蛋白	Lin et al., 2018
	WSL8	白条纹叶	5	脱氧核糖核酸激酶基因	Liu et al., 2020
	V1	温敏白化转绿	3	编码叶绿体定位蛋白NUS1, 参与叶绿体RNA	Kusumi et al., 2011
	V1	温敏白化转绿	3	代谢调节	Kusumi et al., 2011
	V3	白化转绿	6	编码核糖核酸还原酶大亚基	Inagaki et al., 2015
	V4	低温白化	7	编码PPR蛋白	Lv et al., 2020
	TCD5	温敏白化	5	单加氧酶基因	Wang et al., 2016a
	GARS	白条纹叶	8	编码一种催化嘌呤核苷酸生物合成第2步的酶	Cao et al., 2018
	YGL8	黄叶	1	编码尿嘧啶核苷酸激酶	Kong et al., 2016
	Rey(k2)	黄化转绿	10	磷酸果糖激酶B型碳水化合物激酶基因	Zhu et al., 2020a