Chin Bull Bot ›› 2017, Vol. 52 ›› Issue (1): 102-112.doi: 10.11983/CBB16222

Special Issue: Rice Biology

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Advances in Understanding Leaf Premature Senescence and Its Molecular Mechanism in Rice

Na Xu, Jiangmin Xu, Linghuan Jiang, Yuchun Rao*   

  1. College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, China
  • Received:2016-11-17 Accepted:2016-12-15 Online:2017-01-23 Published:2017-01-01
  • Contact: Rao Yuchun E-mail:ryc@zjnu.cn
  • About author:

    # Co-first authors

Abstract:

Senescence of plant leaves is the final stage of leaf development as well as a adaptive performance of the long-term evolution of plants. The senescence of rice (Oryza sativa) leaves greatly affects the quality and yield of rice. Study of leaf senescence has mainly focused on pre-senility. This paper reviews the research progress in rice senescence and genes related to rice senescence, especially advanced suggestions about the causes, the process, and physiological changes of rice leaf senescence and how to prevent senescence. These studies establish a theoretical foundation for further analysis of the molecular mechanism of rice premature senescence and provide some reference for rice breeding as well.

Figure 1

The stages of premature senescence and possible ways"

Table 1

A part of cloned leaf premature senescence-related genes in rice"

基因功能类别 基因名称 基因的可能功能 参考文献
叶绿体的发育及叶绿素降解 SGR 叶绿素降解 Jiang et al., 2007
OsPAO 脱植基叶绿素氧化酶 Tang et al., 2011
Ygl1 该基因突变使叶绿体合成的最后一步
脂化反应受损, 幼苗期叶片黄化
Wu et al., 2007
Oslms 双链RNA结合蛋白 Undan et al., 2012
Ospse1 果胶分解酶 Wu et al., 2013
PSL2 糖基转移酶 孙玉莹, 2013
GS1(胞质内)、GS2(叶绿体内) 谷氨酞合成酶 Pageau et al., 2006
SUR1 乙醛酸氧化酶 张丽霞, 2000
SURSUR3 金属硫蛋白
蛋白质合成、降解及转运 GnT1 N-乙酰葡糖氨基转移酶 Fananta et al., 2013
途径 OsSAG12-1 半胱氨酸蛋白酶前体 Singh et al., 2013
Osl20 支链α-酮酸脱氢酶
Osl30 4-羟基苯双加氧酶
Osl43 盐诱导蛋白
Osl55 丙氨酸-乙醛酸氨基转移酶 Lee et al., 2001
Osl57 三酰辅酶A硫解酶
Osl85 异柠檬酸裂解酶
Osl139 种子蛋白
Osl295 天冬氨酸蛋白酶
Osl381 dTDP-葡萄糖4,6脱水酶
Osh36 氨基转移酶 Lee et al., 2004
Osh69 碱性α-半乳糖苷酶
激素途径 OsHox33 III类同源域亮氨酸拉链 Luan et al., 2013
细胞程序性死亡途径 SPL28 网格型衔接蛋白复合物1的中间亚基μ1 Qiao et al., 2010
OsCATC 过氧化氢酶 Lin et al., 2012
其它 Spl11 抗真菌(E3连接酶) Zeng et al., 2004
OsNAP NAC家族的转录因子 Liang et al., 2014
Osh67Osh70 未知功能, 聚糖醛酸酶同工酶1的β-亚基 Lee et al., 2001
OsSAP 衰老相关蛋白 Ubaidillah et al., 2013
ONAC106 调节信号通路靶基因的表达 Sakuraba et al., 2015
[1] 曹显祖, 朱庆森 (1981). 提高杂交稻结实率的中间试验. 江苏农业科学 5, 5-6.
[2] 丁世琪, 吴洪恺 (2011). 植物早衰的分子机理研究进展. 杂交水稻 26, 1-5.
[3] 方立魁, 李云峰, 龚小平, 桑贤春, 凌英华, 王晓雯, 丛云飞, 何光华 (2010). 水稻叶片显性早衰突变体psl3的遗传分析与基因精细定位. 科学通报 55, 1676-1681.
[4] 李静, 沈法富, 于东海 (2004). 植物衰老中的编程性细胞死亡. 植物学通报 21, 724-732.
[5] 沈年伟, 钱前, 张光恒 (2009). 水稻卷叶性状的研究进展及在育种中的应用. 分子植物育种 7, 852-860.
[6] 孙玉莹 (2013). 水稻叶片早衰基因PSL2的图位克隆及功能初步分析. 北京: 作物科学研究所. pp. 11-36.
[7] 吴书俊, 杨姐, 闫影, 张丽霞, 范方军, 朱金燕, 李文奇, 仲维功, 曹黎明 (2015). 水稻黄绿叶突变体ygl11(t)的生理特性和基因克隆. 中国水稻科学 29, 111-118.
[8] 徐芳芳, 桑贤春, 任德勇, 唐彦强, 胡宏伟, 杨正林, 赵芳明, 何光华 (2012). 水稻早衰突变体esl2的遗传分析及基因定位. 作物学报 38, 1347-1353.
[9] 严雯奕, 叶胜海, 董彦君, 金庆生, 张小明 (2010). 植物叶片衰老相关研究进展. 作物杂志 4, 4-9.
[10] 杨同文, 李成伟 (2014). 植物叶片衰老的表观遗传调控. 植物学报 49, 729-737.
[11] 杨窑龙, 饶玉春, 刘慧娟, 方云霞, 董国军, 黄李超, 冷语佳, 郭龙彪, 张光恒, 胡江, 高振宇, 钱前, 曾大力 (2011). 水稻早衰叶突变体es-t的遗传分析与精细定位. 科学通报 56, 1539-1545.
[12] 袁明, 瞿礼嘉, 王小菁, 钱前, 杨维才, 王台, 孔宏智, 蒋高明, 种康 (2014). 2013年中国植物科学若干领域重要研究进展. 植物学报 49, 347-406.
[13] 翟荣荣, 冯跃, 曹立勇, 程式华, 吴伟明 (2011). 水稻叶片衰老研究进展. 中国稻米 17, 7-12.
[14] 张丽霞 (2000). 水稻叶片衰老相关基因的分离. 福州: 福建农业大学. pp. 46-49.
[15] 张荣铣, 戴新宾, 许晓明 (1999). 叶片光合功能期与作物光合生产潜力. 南京师范大学学报 22, 376-386.
[16] Andres C, Agne B, Kessler F (2010). The TOC complex: perprotein gateway to the chloroplast.Biochim Biophys Acta 1803, 715-723.
[17] Asada K (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions.Plant Physiol 141, 391-396.
[18] Bielen A, Remans T, Vangronsveld J, Cuypers A (2013). The influence of metal stress on the availability and redox state of ascorbate, and possible interference with its cellular functions.Int J Mol Sci 3, 6382-6413.
[19] Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003). The molecular analysis of leaf senescence genomics approach. Plant Biotechnol J 1, 3-22.
[20] Chae H, Lee W (2002). Ethylene- and enzyme-mediated superoxide production and cell death in carrot cells grown under carbon starvation.Plant Cell Rep 20, 256-261.
[21] Delorme VG, McCabe PF, Kim DJ, Leaver CJ (2000). A matrix metalloproteinase gene is expressed at the boun- dary of senescence and programmed cell death in cucumber.Plant Physiol 123, 917-927.
[22] Dominique L, Jean CB (1998). High levels of antioxidant enzymes correlate with delayed senescence in nonnetted muskmelon fruits.Planta 204, 377-382.
[23] Fanata WI, Lee KH, Son BH, Yoo JY, Harmoko R, Ko KS, Ramasamy NK, Kim KH, Oh DB, Jung HS, Kim JY, Lee SY, Lee KO (2013). N-glycan maturation is crucial for cytokinin-mediated development and cellulose synthesis in Oryza sativa.Plant J 73, 966-979.
[24] Fang C, Zhang H, Wan J, Wu Y, Li K, Jin C, Chen W, Wang S, Wang W, Zhang H, Zhang P, Zhang F, Qu L, Liu X, Zhou DX, Luo J (2016). Control of leaf senescence by an MeOH-jasmonates cascade that is epigene- tically regulated by OsSRT1 in rice.Mol Plant 9, 1366-1378.
[25] Fukao T, Yeung E, Bailey-Serres J (2012). The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice.Plant Physiol 160, 1795-1807.
[26] Gregersen PL, Culetic A, Boschian L, Krupinska K (2013). Plant senescence and crop productivity.Plant Mol Biol 82, 603-622.
[27] Guo Y, Gan SS (2012). Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments.Plant Cell Environ 35, 644-655.
[28] He Y, Gan S (2002). A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis.Plant Cell 14, 805-815.
[29] Helmann H, Estelle M (2002). Plant development: regulation by protein degradation.Science 297, 793-797.
[30] Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011). LEAF TIP NECROSIS1 plays a pivotal role in regulation of multiple phosphate starvation res- ponses in rice.Plant Physiol 156, 1101-1115.
[31] Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008). Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process.Plant Physiol 148, 142-155.
[32] 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, 197-209.
[33] Jiao BB, Wang JJ, Zhu XD, Zeng LJ, Li Q, He ZH (2012). A novel protein RLS1 with NB-ARM domains is involved in chloroplast degradation during leaf senescence in rice.Mol Plant 5, 205-217.
[34] Jibran R, A Hunter D, P Dijkwel P (2013). Hormonal regulation of leaf senescence through integration of development and stress signals.Plant Mol Biol 82, 547-561.
[35] Kim HJ, Nam HG, Lim PO (2016a). Regulatory network of NAC transcription factors in leaf senescence.Curr Opin Plant Biol 33, 48-56.
[36] Kim J, Woo HR, Nam HG (2016b). Toward systems understanding of senescence: an integrated multi-omics perspective on leaf senescence research.Mol Plant 9, 813-825.
[37] Kovács-Bogdán E, Soll J, Bolter B (2010). Protein import into chloroplasts: the Tic complex and its regulation.Biochim Biophys Acta 1803, 740-747.
[38] Kusaba M, Tanaka A, Tanaka R (2013). Stay-green plants: what do they tell us about the molecular mrchanism of leaf senescence.Photosynth Res 117, 221-234.
[39] Lai X, Beilharz T, Au WC, Hammet A, Preiss T, Basrai MA, Heierhorst J (2013). Yeast hEST1A/B (SMG5/6)-like proteins contribute to environment-sensing adaptive gene expression responses. G3 (Bethesda) 3, 1649-1659.
[40] Lee RH, Lin MC, Chen SC (2004). A novel alkaline α-galac- tosidase gene is involved in rice leaf senescence.Mol Biol 55, 281-295.
[41] Lee RH, Wang CH, Huang LT, Chen SC (2001). Leaf senescence in rice plants: cloning and characterization of senescence up regulated genes.J Exp Bot 52, 1117-1121.
[42] Li X, Li JH, Wang W, Chen NZ, Ma TS, Xi YN, Zhang XL, Lin HF, Bai Y, Huang SJ, Chen YL (2014). ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis.Plant Cell Environ 37, 1548-1560.
[43] Liang C, Chu C (2015). Towards understanding abscisic acid-mediated leaf senescence.Sci China Life Sci 58, 506-508.
[44] Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C (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 USA 111, 10013-10018.
[45] Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu XG, Tan DX, Chen SY, Chu C (2015). Melatonin delays leaf senescence and enhances salt stress tolerance in rice.J Pineal Res 59, 91-101.
[46] Lim PO, Woo HR, Nam HG (2003). Molecular genetics of leaf senescence in Arabidopsis.Trends Plant Sci 8, 272-278.
[47] Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012). Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice.Plant Physiol 158, 451-464.
[48] Luan W, Shen A, Jin Z, Song S, Li Z, Sha A (2013). Kon- ckdown of OsHox33, a member of the class III homeodomain-leucine zipper gene family, accelerates leaf senescence in rice.Sci China Life Sci 56, 1113-1123.
[49] Mao D, Yu H, Liu T, Yang G, Xing Y (2011). Two complementary recessive genes in duplicated segments control etiolation in rice.Theor Appl Genet 122, 373-383.
[50] Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B (2000). Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence.Planta 211, 510-518.
[51] Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003). Role of the Arabidopsis glucose seneor HXK1 in nutrient, light, and hormonal signaling.Science 300, 332-336.
[52] Noodén LD, Guiamet JJ, John I (1997). Senescence mechanisms.Plant Physiol 101, 746-753.
[53] Pageau K, Reisdorf-Cren M, Morot-Gaudry JF, Masclaux- Daubresse C (2006). The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves.J Exp Bot 57, 547-557.
[54] Pan YJ, Liu L, Lin YC, Zu YG, Li LP, Tang ZH (2016). Ethylene?antagonizes salt-induced growth retardation and cell death process via transcriptional controlling of?ethylene-, BAG- and?senescence-sssociated genes in Ara- bidopsis.Front?Plant?Sci 7, 696.
[55] Panda D, Sarkar RK (2013). Natural leaf senescence: probed by chlorophyII fluorescence, CO2 photosynthetic rate and antioxidant enzyme activities during grain filling in different rice cultivars.Physiol Mol Biol Plants 19, 43-51.
[56] Qiao Y, Jiang W, Lee J, Park B, Choi MS, Piao R, Woo MO, Roh JH, Han L, Paek NC, Seo HS, Koh HI (2010). SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit micro 1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa).New Phytol 185, 258-274.
[57] Quirino BF, Reiter WD, Amasino RD (2001). One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated.Plant Mol Biol 46, 447-457.
[58] Rao Y, Yang Y, Xu J, Li X, Leng Y, Dai L, Huang L, Shao G, Ren D, Hu J, Guo L, Pan J, Zeng D (2015). EARLY SENESCENCE 1 encodes a SCAR-like protein 2 that affects water loss in rice.Plant Physiol 169, 1225-1239.
[59] Riefler M, Novak O, Strnad M, Schmülling T (2006). Ara- bidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism.Plant Cell 18, 40-54.
[60] Rolland F, Moore B, Sheen J (2002). Sugar sensing and signaling in plants.Plant Cell (suppl), S185-S205.
[61] Sakuraba Y, Balazadeh S, Tanaka R, Mueller-Roeber B, Tanaka A (2012). Overproduction of chl B retards senescence through transcriptional reprogramming in Arabi- dopsis.Plant Cell Physiol 53, 505-517.
[62] Sakuraba Y, Piao W, Lim JH, Han SH, Kim YS, An G, Paek NC (2015). Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle.Plant Cell Physiol 56, 2325-2339.
[63] Schippers JH (2015). Transcriptional networks in leaf senescence.Curr Opin Plant Biol 27, 77-83.
[64] Simeonova E, Sikora A, Charzyska M, Mostowska A (2000). Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants.Protoplasma 214, 93-101.
[65] Singh S, Giri MK, Singh PK, Siddiqui A, Nandi AK (2013). Down-regulation of OsSAG12-1 results in enhanced senescence and pathogen-induced cell death in transgenic rice plants.J Biosci 38, 583-592.
[66] Stessman D, Miller A, Spalding M, Rodermel S (2002). Regulation of photosynthesis during Arabidopsis leaf development in continuous light.Photosynth Res 72, 27-37.
[67] Tang Y, Li M, Chen Y, Wu P, Wu G, Jiang H (2011). Konckdown of OsPAO and OSRCCR1 cause different plant death phenotypes in rice.J Plant Physiol 168, 1952-1959.
[68] Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003). Defining senescence and death.J Exp Bot 54, 1127-1232.
[69] Ubaidillah M, Kim KA, Kim YH, Lee IJ, Yun BW, Kim DH, Loake GJ, Kim KM (2013). Identification of a drought rice gene, OsSAP, that suppresses Bax-induced cell death in yeast.Mol Biol Rep 40, 6113-6121.
[70] Undan JR, Tamiru M, Abe A, Yoshida K, Kosugi S, Takagi H, Yoshida K, Kanzaki H, Saitoh H, Fekih R, Sharma S, Undan J, Yano M, Terauchi R (2012). Mutation in OsLMS, a gene encoding a protein with two double-stranded RNA binding motifs, causes lesion mimic phenotype and early senescence in rice (Oryza sativa L.).Genes Genet Sys 87, 169-179.
[71] Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009). Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves.Plant Physiol 149, 885-893.
[72] Wingler A, Purdy S, Maclean JA, Pourtau N (2006). The role of sugars in integrating environmental signals during the regulation of leaf senescence.J Exp Bot 57, 391-399.
[73] Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001). ORE9, an F-box protein that regulates leaf senescence in Arabidopsis.Plant Cell 13, 1779-1790.
[74] Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B, Kim YW, Phee BK, Kim JH, Seo C, Park C, Kim SC, Park S, Lee B, Lee S, Hwang D, Nam HG, Lim PO (2016). Programming of?plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis.Plant Phy- siol 171, 452-467.
[75] Wu HB, Wang B, Chen Y, Liu YG, Chen L (2013). Characterization and fine mapping of the rice premature senescence mutant ospse1. Theor Appl Genet 126, 1897-1907.
[76] Wu L, Ren D, Hu S, Li G, Dong G, Jiang L, Hu X, Ye W, Cui Y, Zhu L, Hu J, Zhang G, Gao Z, Zeng D, Qian Q, Guo L (2016). Down-regulation of a nicotinate phos- phoribosyltransferase gene, OsNaPRT1, leads to withered leaf tips.Plant Physiol 171, 1085-1098.
[77] Wu Z, Zhang X, He B, Diao L, Sheng S, Wang J, Guo X, Su N, Wang L, Jiang L, Wang C, Zhai H, Wan J (2007). A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis.Plant Physiol 145, 29-40.
[78] Xiao W, Sheen J, Jang JC (2000). The role of hexokinase in plant sugar signal transduction and growth and development.Plant Mol Biol 44, 451-461.
[79] Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002). A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein.Proc Natl Acad Sci USA 99, 7530-7535.
[80] Yan WY, Ye SH, Jin QS (2010). Characterization and mapping of novel mutant sms1 (senescence and male sterility 1) in rice.J Genet Genomics 37, 47-55.
[81] Yang D, Li Y, Shi Y, Cui Z, Luo Y, Zheng M, Chen J, Li Y, Yin Y, Wang Z (2016a). Exogenous cytokinins increase grain yield of winter wheat cultivars by improving stay-green characteristics under heat stress.PLoS One 11, e0155437.
[82] Yang SQ, Li WQ, Miao H, Gan PF, Qiao L, Chang YL, Shi CH, Chen KM (2016b). REL2, a gene encoding an unknown function protein which contains DUF630 and DUF632 domains controls leaf rolling in rice.Rice 9, 37.
[83] Yang Y, Xu J, Huang L, Leng Y, Dai L, Rao Y, Chen L, Wang Y, Tu Z, Hu J, Ren D, Zhang G, Zhu L, Guo L, Qian Q, Zeng D (2016c). PGL, encoding chlorophyllide a oxygenase 1, impacts leaf senescence and indirectly affects grain yield and quality in rice. J Exp Bot 67, 1297-1310.
[84] Yoshida S (2003). Molecular regulation of leaf senescence.Curr Opin Plant Biol 6, 79-84.
[85] Yoshida S, Ito M, Callis J, Nishida I, Watanabe A (2002). A delayed leaf senescence mutant is defective in arginyl tRNA: protein arginyltransferase, a component of the N end rule pathway in Arabidopsis.Plant J 32, 129-137.
[86] Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004). Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-Box/Armadillo repeat protein endowed with E3 ubiquitin legase activity. Plant Cell 16, 2795-2808.
[87] Zhang H, Zhou C (2013). Signal transduction in leaf senenscence.Plant Mol Biol 82, 539-545.
[88] Zhang W, Zhou X, Wen CK (2012). Modulation of ethylene responses by OsRTH1 overexpression reveals the biological significance of ethylene in rice seedling growth and development.J Exp Bot 63, 4151-4164.
[89] Zhang Y, Liu J, Chai J, Xing D (2016). Mitogen-activated protein kinase 6 mediates nuclear translocation of ORE3 to promote ORE9 gene expression in methyl jasmonate- induced leaf senescence.J Exp Bot 180, 83-94.
[90] Zhou Y, Huang W, Liu L, Chen T, Zhou F, Lin Y (2013). Identification and functional characterization of a rice NAC gene involved in the regulation of leaf senescence.BMC Plant Biol 13, 132.
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[3] . [J]. Chin Bull Bot, 1994, 11(专辑): 65 .
[4] . [J]. Chin Bull Bot, 1996, 13(专辑): 103 .
[5] ZHANG Xiao-Ying;YANG Shi-Jie. Plasmodesmata and Intercellular Trafficking of Macromolecules[J]. Chin Bull Bot, 1999, 16(02): 150 -156 .
[6] Chen Zheng. Arabidopsis thaliana as a Model Species for Plant Molecular Biology Studies[J]. Chin Bull Bot, 1994, 11(01): 6 -11 .
[7] . [J]. Chin Bull Bot, 1996, 13(专辑): 13 -16 .
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