植物半胱氨酸蛋白酶在植物生长发育中的功能研究

doi:10.13560/j.cnki.biotech.bull.1985.2020-1220

摘要/Abstract

摘要：

半胱氨酸蛋白酶(cysteine proteases,CPs)是一类重要的蛋白水解酶,在调控植物生长发育中发挥着重要的功能。根据不同半胱氨酸蛋白酶在不同组织部位的定位表达,对半胱氨酸蛋白酶参与种子萌发,根生长及叶片衰老过程,以及茎中导管分子及花药中绒毡层细胞的细胞程序性死亡过程的功能研究及其进展进行了综述,旨在为进一步研究半胱氨酸蛋白酶的功能提供参考。

关键词: 半胱氨酸蛋白酶, 细胞程序性死亡(PCD), 叶衰老, 种子萌发

Abstract:

Cysteine proteases are an important class of proteolytic enzymes and play an important role in regulating plant growth and development. Based on the expression patterns of different cysteine proteases in different tissues and organs,this article reviews the functional research and progress of cysteine proteases involved in seed germination,root development,leaf senescence,programmed cell death of tracheary elements in stems and of tapetum in anthers,aiming to provide references for further studying the function of cysteine protease.

Key words: cysteine protease, programmed cell death, leaf senescence, seed germination

莫黎杰, 刘夏瞳, 李慧, 陆海. 植物半胱氨酸蛋白酶在植物生长发育中的功能研究[J]. 生物技术通报, 2021, 37(6): 202-212.

MO Li-jie, LIU Xia-tong, LI Hui, LU Hai. On the Function of Plant Cysteine Protease in Plant Growth and Development[J]. Biotechnology Bulletin, 2021, 37(6): 202-212.

图/表 1

参考文献 88

[1]	van der Hoorn RA, Jones JD. The plant proteolytic machinery and its role in defence[J]. Curr Opin Plant Biol, 2004, 7(4):400-407. doi: 10.1016/j.pbi.2004.04.003 URL
[2]	van der Hoorn RA. Plant proteases:from phen otypes to molecular mechanisms[J]. Annu Rev Plant Biol, 2008, 59:191-223. doi: 10.1146/annurev.arplant.59.032607.092835 URL
[3]	Grudkowska M, Zagdańska B. Multifunctional role of plant cysteine proteinases[J]. Acta Biochim Pol, 2004, 51(3):609-624. doi: 10.18388/abp.2004_3547 URL
[4]	Rawlings ND, Barrett AJ, Finn R. Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors[J]. Nucleic Acids Res, 2016, 44(D1):D343-D350. doi: 10.1093/nar/gkv1118 URL
[5]	Rawlings ND, Waller M, Barrett AJ, et al. MEROPS:the database of proteolytic enzymes, their substrates and inhibitors[J]. Nucleic Acids Res, 2014, 42(Database issue):D503-D509. doi: 10.1093/nar/gkt953 URL
[6]	Rawlings ND, Morton FR, Barrett AJ. MEROPS:the peptidase database[J]. Nucleic Acids Res, 2006, 34(Database issue):D270-D272. doi: 10.1093/nar/gkj089 URL
[7]	Rawlings ND, Barrett AJ, Bateman A. MEROPS:the peptidase database[J]. Nucleic Acids Res, 2010, 38(Database issue):D227-D233. doi: 10.1093/nar/gkp971 URL
[8]	Polgár L, Halász P. Current problems in mechanistic studies of serine and cysteine proteinases[J]. Biochem J, 1982, 207(1):1-10. pmid: 6758764
[9]	Richau KH, Kaschani F, Verdoes M, et al. Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics[J]. Plant Physiol, 2012, 158(4):1583-1599. doi: 10.1104/pp.112.194001 URL
[10]	Krupinska K, Mulisch M, Hollmann J, et al. An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley[J]. Physiol Plant, 2012, 144(2):189-200. doi: 10.1111/j.1399-3054.2011.01545.x pmid: 22098170
[11]	McLellan H, Gilroy EM, Yun BW, et al. Functional redundancy in the Arabidopsis Cathepsin B gene family contributes to basal defence, the hypersensitive response and senescence[J]. New Phytol, 2009, 183(2):408-418. doi: 10.1111/nph.2009.183.issue-2 URL
[12]	Velasco-Arroyo B, Diaz-Mendoza M, Gandullo J, et al. HvPap-1 C1A protease actively participates in barley proteolysis mediated by abiotic stresses[J]. J Exp Bot, 2016, 67(14):4297-4310. doi: 10.1093/jxb/erw212 pmid: 27217548
[13]	Bhalerao R, Keskitalo J, Sterky F, et al. Gene expression in autumn leaves[J]. Plant Physiol, 2003, 131(2):430-442. pmid: 12586868
[14]	Liu H, Hu M, Wang Q, et al. Role of papain-like cysteine proteases in plant development[J]. Front Plant Sci, 2018, 9:1717. doi: 10.3389/fpls.2018.01717 URL
[15]	Lohman KN, Gan S, John MC, et al. Molecular analysis of natural leaf senescence in Arabidopsis thaliana[J]. Physiologia Plantarum, 1994, 92(2):322-328. doi: 10.1111/ppl.1994.92.issue-2 URL
[16]	Yamada K, Matsushima R, Nishimura M, et al. A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves[J]. Plant Physiol, 2001, 127(4):1626-1634. pmid: 11743107
[17]	Pruzinska A, Shindo T, Niessen S, et al. Major Cys protease activities are not essential for senescence in individually darkened Arabidopsis leaves[J]. BMC Plant Biol, 2017, 17(1):4. doi: 10.1186/s12870-016-0955-5 URL
[18]	Díaz-Mendoza M, Velasco-Arroyo B, González-Melendi P, et al. C1A cysteine protease-cystatin interactions in leaf senescence[J]. J Exp Bot, 2014, 65(14):3825-3833. doi: 10.1093/jxb/eru043 pmid: 24600023
[19]	Desclos M, Etienne P, Coquet L, et al. A combined ¹⁵N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation[J]. Proteomics, 2009, 9(13):3580-3608. doi: 10.1002/pmic.200800984 pmid: 19609964
[20]	Beyene G, Foyer CH, Kunert KJ. Two new cysteine proteinases with specific expression patterns in mature and senescent tobacco(Nicotiana tabacum L.)leaves[J]. J Exp Bot, 2006, 57(6):1431-1443. pmid: 16551685
[21]	Carrión CA, Costa ML, Martínez DE, et al. In vivo inhibition of cysteine proteases provides evidence for the involvement of ‘senescence-associated vacuoles’ in chloroplast protein degradation during dark-induced senescence of tobacco leaves[J]. J Exp Bot, 2013, 64(16):4967-4980. doi: 10.1093/jxb/ert285 URL
[22]	Liu L, Zhou Y, Szczerba MW, et al. Identification and application of a rice senescence-associated promoter[J]. Plant Physiol, 2010, 153(3):1239-1249. doi: 10.1104/pp.110.157123 pmid: 20439547
[23]	Zou Z, Liu J, Yang L, et al. Survey of the rubber tree genome reveals a high number of cysteine protease-encoding genes homologous to Arabidopsis SAG12[J]. PLoS One, 2017, 12(2):e0171725. doi: 10.1371/journal.pone.0171725 URL
[24]	Xiao HJ, Yin YX, Chai WG, et al. Silencing of the CaCP gene delays salt- and osmotic-induced leaf senescence in Capsicum annuum L.[J]. Int J Mol Sci, 2014, 15(5):8316-8334. doi: 10.3390/ijms15058316 URL
[25]	Noh YS, Amasino RM. Identification of a promoter region responsible for the senescence-specific expression of SAG12[J]. Plant Mol Biol, 1999, 41(2):181-194. pmid: 10579486
[26]	Weaver LM, Gan S, Quirino B, et al. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment[J]. Plant Mol Biol, 1998, 37(3):455-469. pmid: 9617813
[27]	Zhang K, Halitschke R, Yin C, et al. Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism[J]. Proc Natl Acad Sci USA, 2013, 110(36):14807-14812. doi: 10.1073/pnas.1302702110 URL
[28]	Li Z, Peng J, Wen X, et al. Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis[J]. Plant Cell, 2013, 25(9):3311-3328. doi: 10.1105/tpc.113.113340 URL
[29]	Otegui MS, Noh YS, Martínez DE, et al. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean[J]. Plant J, 2005, 41(6):831-844. doi: 10.1111/tpj.2005.41.issue-6 URL
[30]	James M, Poret M, Masclaux-Daubresse C, et al. SAG12, a major cysteine protease involved in nitrogen allocation during senescence for seed production in Arabidopsis thaliana[J]. Plant Cell Physiol, 2018, 59(10):2052-2063. doi: 10.1093/pcp/pcy125 URL
[31]	Poret M, Chandrasekar B, van der Hoorn RAL, et al. Characterization of senescence-associated protease activities involved in the efficient protein remobilization during leaf senescence of winter oilseed rape[J]. Plant Sci, 2016, 246:139-153. doi: 10.1016/j.plantsci.2016.02.011 URL
[32]	James M, Masclaux-Daubresse C, Marmagne A, et al. A new role for SAG12 cysteine protease in roots of Arabidopsis thaliana[J]. Front Plant Sci, 2019, 9:1998. doi: 10.3389/fpls.2018.01998 URL
[33]	Singh S, Giri MK, Singh PK, et al. Down-regulation of OsSAG12-1 results in enhanced senescence and pathogen-induced cell death in transgenic rice plants[J]. J Biosci, 2013, 38(3):583-592. doi: 10.1007/s12038-013-9334-7 URL
[34]	Singh S, Singh A, Nandi AK. The rice OsSAG12-2 gene codes for a functional protease that negatively regulates stress-induced cell death[J]. J Biosci, 2016, 41(3):445-453. doi: 10.1007/s12038-016-9626-9 URL
[35]	Gomez-Sanchez A, Gonzalez-Melendi P, Santamaria ME, et al. Repression of drought-induced cysteine-protease genes alters barley leaf structure and responses to abiotic and biotic stresses[J]. J Exp Bot, 2019, 70(7):2143-2155. doi: 10.1093/jxb/ery410 pmid: 30452688
[36]	Hollmann J, Gregersen PL, Krupinska K. Identification of predominant genes involved in regulation and execution of senescence-associated nitrogen remobilization in flag leaves of field grown barley[J]. J Exp Bot, 2014, 65(14):3963-3973. doi: 10.1093/jxb/eru094 pmid: 24700620
[37]	Frank S, Hollmann J, Mulisch M, et al. Barley cysteine protease PAP14 plays a role in degradation of chloroplast proteins[J]. J Exp Bot, 2019, 70(21):6057-6069. doi: 10.1093/jxb/erz356 URL
[38]	Roberts K, McCann MC. Xylogenesis:the birth of a corpse[J]. Curr Opin Plant Biol, 2000, 3(6):517-522. pmid: 11074384
[39]	Kuriyama H, Fukuda H. Developmental programmed cell death in plants[J]. Curr Opin Plant Biol, 2002, 5(6):568-573. pmid: 12393021
[40]	Minami A, Fukuda H. Transient and specific expression of a cysteine endopeptidase associated with autolysis during differentiation of Zinnia mesophyll cells into tracheary elements[J]. Plant Cell Physiol, 1995, 36(8):1599-1606. pmid: 8589934
[41]	Ye ZH, Varner JE. Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans[J]. Plant Mol Biol, 1996, 30(6):1233-1246. pmid: 8704132
[42]	Yamamoto R, Demura T, Fukuda H. Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells[J]. Plant Cell Physiol, 1997, 38(8):980-983. pmid: 9440936
[43]	Demura T, Tashiro G, Horiguchi G, et al. Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells[J]. Proc Natl Acad Sci USA, 2002, 99(24):15794-15799. doi: 10.1073/pnas.232590499 URL
[44]	Pyo H, Demura T, Fukuda H. Spatial and temporal tracing of vessel differentiation in young Arabidopsis seedlings by the expression of an immature tracheary element-specific promoter[J]. Plant Cell Physiol, 2004, 45(10):1529-1536. doi: 10.1093/pcp/pch175 URL
[45]	Pyo H, Demura T, Fukuda H. TERE;a novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements[J]. Plant J, 2007, 51(6):955-965. doi: 10.1111/j.1365-313X.2007.03180.x URL
[46]	Funk V, Kositsup B, Zhao C, et al. The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog[J]. Plant Physiol, 2002, 128(1):84-94. doi: 10.1104/pp.010514 URL
[47]	Avci U, Earl Petzold H, Ismail IO, et al. Cysteine proteases XCP1 and XCP2 aid micro-autolysis within the intact central vacuole during xylogenesis in Arabidopsis roots[J]. Plant J, 2008, 56(2):303-315. doi: 10.1111/j.1365-313X.2008.03592.x URL
[48]	Yamada K, Shimada T, Nishimura M, et al. A VPE family supporting various vacuolar functions in plants[J]. Physiol Plant, 2005, 123(4):369-375. doi: 10.1111/ppl.2005.123.issue-4 URL
[49]	Gruis D, Schulze J, Jung R. Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases[J]. Plant Cell, 2004, 16(1):270-290. doi: 10.1105/tpc.016378 URL
[50]	Kinoshita T, Yamada K, Hiraiwa N, et al. Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions[J]. Plant J, 1999, 19(1):43-53. pmid: 10417725
[51]	Han J, Li H, Yin B, et al. The papain-like cysteine protease CEP1 is involved in programmed cell death and secondary wall thickening during xylem development in Arabidopsis[J]. J Exp Bot, 2019, 70(1):205-215. doi: 10.1093/jxb/ery356 URL
[52]	Cheng Z, Zhang J, Yin B, et al. γVPE plays an important role in programmed cell death for xylem fiber cells by activating protease CEP1 maturation in Arabidopsis thaliana[J]. Int J Biol Macromol, 2019, 137:703-711. doi: S0141-8130(19)32298-6 pmid: 31279878
[53]	Mikkonen A, Porali I, Cercos M, et al. A major cysteine proteinase, EPB, in germinating barley seeds:structure of two intronless genes and regulation of expression[J]. Plant Mol Biol, 1996, 31(2):239-254. pmid: 8756590
[54]	Prabucka B, Drzymała A, Grabowska A. Molecular cloning and expression analysis of the main gliadin-degrading cysteine endopeptidase EP8 from triticale[J]. Cereal Sci, 2013, 58(2):284-289. doi: 10.1016/j.jcs.2013.06.004 URL
[55]	Szewińska J, Simińska J, Bielawski W. The roles of cysteine proteases and phytocystatins in development and germination of cereal seeds[J]. J Plant Physiol, 2016, 207:10-21. doi: 10.1016/j.jplph.2016.09.008 URL
[56]	Zhang N, Jones BL. Characterization of germinated barley endoproteolytic enzymes by two dimensional gel electrophoresis[J]. Cereal Sci, 1995, 21(2):145-153. doi: 10.1016/0733-5210(95)90030-6 URL
[57]	Tan-Wilson AL, Wilson KA. Mobilization of seed protein reserves[J]. Physiol Plant, 2012, 145(1):140-153. doi: 10.1111/j.1399-3054.2011.01535.x pmid: 22017287
[58]	Kuo A, Cappelluti S, Cervantes-Cervantes M, et al. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells[J]. Plant Cell, 1996, 8(2):259-269. pmid: 8742711
[59]	Sreenivasulu N, Usadel B, Winter A, et al. Barley grain maturation and germination:metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools[J]. Plant Physiol, 2008, 146(4):1738-1758. doi: 10.1104/pp.107.111781 pmid: 18281415
[60]	Rogers JC, Dean D, Heck GR. Aleurain:a barley thiol protease closely related to mammalian cathepsin H[J]. Proc Natl Acad Sci USA, 1985, 82(19):6512-6516. doi: 10.1073/pnas.82.19.6512 URL
[61]	Cambra I, Martinez M, Dáder B, et al. A cathepsin F-like peptidase involved in barley grain protein mobilization, HvPap-1, is modulated by its own propeptide and by cystatins[J]. J Exp Bot, 2012, 63(12):4615-4629. doi: 10.1093/jxb/ers137 pmid: 22791822
[62]	Diaz-Mendoza M, Dominguez-Figueroa JD, Velasco-Arroyo B, et al. HvPap-1 C1A protease and HvCPI-2 cystatin contribute to barley grain filling and germination[J]. Plant Physiol, 2016, 170(4):2511-2524. doi: 10.1104/pp.15.01944 pmid: 26912343
[63]	Martinez M, Cambra I, Carrillo L, et al. Characterization of the entire cystatin gene family in barley and their target cathepsin L-like cysteine-proteases, partners in the hordein mobilization during seed germination[J]. Plant Physiol, 2009, 151(3):1531-1545. doi: 10.1104/pp.109.146019 pmid: 19759340
[64]	Sutoh K, Kato H, Minamikawa T. Identification and possible roles of three types of endopeptidase from germinated wheat seeds[J]. J Biochem, 1999, 126(4):700-707. pmid: 10502678
[65]	Wang Y, Hu A, Liu S, et al. The vacuolar processing enzyme OsVPE1 is required for efficient glutelin processing in rice[J]. Plant J, 2009, 58(4):606-617. doi: 10.1111/tpj.2009.58.issue-4 URL
[66]	Ho SL, Tong WF, Yu SM. Multiple mode regulation of a cysteine proteinase gene expression in rice[J]. Plant Physiol, 2000, 122(1):57-66. pmid: 10631249
[67]	Becker C, Senyuk VI, Shutov AD, et al. Proteinase A, a storage-globulin-degrading endopeptidase of vetch(Vicia sativa L.)seeds, is not involved in early steps of storage-protein mobilization[J]. Eur J Biochem, 1997, 248(2):304-312. pmid: 9346282
[68]	Akasofu H, Yamauchi D, Mitsuhashi W, et al. Nucleotide sequence of cDNA for sulfhydryl-endopeptidase(SH-EP)from cotyledons of germinating Vigna mungo seeds[J]. Nucleic Acids Res, 1989, 17(16):6733. pmid: 2780300
[69]	Kardailsky IV, Brewin NJ. Expression of cysteine protease genes in pea nodule development and senescence[J]. Mol Plant Microbe Interact, 1996, 9(8):689-695. doi: 10.1094/MPMI-9-0689 URL
[70]	Koehler SM, Ho TH. Hormonal regulation, processing, and secretion of cysteine proteinases in barley aleurone layers[J]. Plant Cell, 1990, 2(8):769-783. pmid: 2152126
[71]	Cercós M, Gómez-Cadenas A, Ho TH. Hormonal regulation of a cysteine proteinase gene, EPB-1, in barley aleurone layers:cis- and trans-acting elements involved in the co-ordinated gene expression regulated by gibberellins and abscisic acid[J]. Plant J, 1999, 19(2):107-118. doi: 10.1046/j.1365-313X.1999.00499.x URL
[72]	Shimada T, Yamada K, Kataoka M, et al. Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana[J]. J Biol Chem, 2003, 278(34):32292-32299. pmid: 12799370
[73]	Nakaune S, Yamada K, Kondo M, et al. A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development[J]. Plant Cell, 2005, 17(3):876-887. pmid: 15705955
[74]	Hierl G, Höwing T, Isono E, et al. Ex vivo processing for maturation of Arabidopsis KDEL-tailed cysteine endopeptidase 2(AtCEP2)pro-enzyme and its storage in endoplasmic reticulum derived organelles[J]. Plant Mol Biol, 2014, 84(6):605-620. doi: 10.1007/s11103-013-0157-6 URL
[75]	Helm M, Schmid M, Hierl G, et al. KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds[J]. Am J Bot, 2008, 95(9):1049-1062. doi: 10.3732/ajb.2007404 URL
[76]	Zhou L, Höwing T, Müller B, et al. Expression analysis of KDEL-CysEPs programmed cell death markers during reproduction in Arabidopsis[J]. Plant Reprod, 2016, 29(3):265-272. doi: 10.1007/s00497-016-0288-4 URL
[77]	Höwing T, Dann M, Müller B, et al. The role of KDEL-tailed cysteine endopeptidases of Arabidopsis(AtCEP2 and AtCEP1)in root development[J]. PLoS One, 2018, 13(12):e0209407. doi: 10.1371/journal.pone.0209407 URL
[78]	张强. 毛果杨五个半胱氨酸蛋白酶的表达与功能研究[D]. 北京:北京林业大学, 2016.
	Zhang Q. Expression and function research of five cysteine from Populus trichocarpa Torr. & Gray[D]. Beijing:Beijing Forestry University, 2016.
[79]	Schmid M, Simpson DJ, Sarioglu H, et al. The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum[J]. Proc Natl Acad Sci USA, 2001, 98(9):5353-5358. doi: 10.1073/pnas.061038298 URL
[80]	Zhang X, Wang Y, Lv X, et al. NtCP56, a new cysteine protease in Nicotiana tabacum L., involved in pollen grain development[J]. J Exp Bot, 2009, 60(6):1569-1577. doi: 10.1093/jxb/erp022 URL
[81]	Li D, Xue J, Zhu J, et al. Gene regulatory network for tapetum development in Arabidopsis thaliana[J]. Front Plant Sci, 2017, 8:1559. doi: 10.3389/fpls.2017.01559 URL
[82]	Yang Y, Dong C, Yu J. Cysteine Protease 51(CP51), an anther-specific cysteine protease gene, is essential for pollen exine formation in Arabidopsis[J]. Plant Cell Tiss Organ Cult, 2014, 119(2):383-397. doi: 10.1007/s11240-014-0542-0 URL
[83]	Zhang D, Liu D, Lv X, et al. The cysteine protease CEP1, a key executor involved in tapetal programmed cell death, regulates pollen development in Arabidopsis[J]. Plant Cell, 2014, 26(7):2939-2961. doi: 10.1105/tpc.114.127282 URL
[84]	Cheng Z, Guo X, Zhang J, et al. βVPE is involved in tapetal degradation and pollen development by activating proprotease maturation in Arabidopsis thaliana[J]. J Exp Bot, 2020, 71(6):1943-1955. doi: 10.1093/jxb/erz560 pmid: 31858133
[85]	Song L, Zhou Z, Tang S, et al. Ectopic expression of BnaC. CP20. 1 results in premature tapetal programmed cell death in Arabidopsis[J]. Plant Cell Physiol, 2016, 57(9):1972-1984. doi: 10.1093/pcp/pcw119 URL
[86]	Lee S, Jung KH, An G, et al. Isolation and characterization of a rice cysteine protease gene, OsCP1, using T-DNA gene-trap system[J]. Plant Mol Biol, 2004, 54(5):755-765. doi: 10.1023/B:PLAN.0000040904.15329.29 URL
[87]	Sanders PM, Bui AQ, Weterings K, et al. Anther developmental defects in Arabidopsis thaliana male-sterile mutants[J]. Sex Plant Reprod, 1999, 11(6):297-322. doi: 10.1007/s004970050158 URL
[88]	Grbic V. Spatial expression pattern of SAG12:GUS transgene in tobacco(Nicotiana tabacum)[J]. Physiologia Plantarum, 2010, 116(3):416-422. doi: 10.1034/j.1399-3054.2002.1160318.x URL

生长发育过程 Function	酶种类 Cysteine proteases	物种 Species	文献 Reference
叶衰老过程 Leaf senescence	SAG12	拟南芥Arabidopsis	[15]
	BnSAG12	油菜Napus	[19]
	NtSAG12	烟草Nicotiana tabacum L.	[21]
	OsSAG12-1	水稻Oryza sativa L.	[33]
	OsSAG12-2	水稻Oryza sativa L.	[34]
	HvPap-1/HvPap-19	大麦Hordeum vulgare L.	[18]
	HvPAP-14	大麦Hordeum vulgare L.	[37]
维管组织的PCD过程 Programmed cell death of vascular organization	ZCP4	百日草Zinnia	[40-41]
	AtXCP1/AtXCP2	拟南芥Arabidopsis	[46-47]
	γVPE	拟南芥Arabidopsis	[49-50,52]
种子萌发过程 Seed germination	EPA	大麦Hordeum vulgare L.	[58]
	EPB	大麦Hordeum vulgare L.	[53-54]
	HvPap-1	大麦Hordeum vulgare L.	[61-62]
	βVPE	拟南芥Arabidopsis	[48]
	δVPE	拟南芥Arabidopsis	[72]
	HvPap-4/HvPap-6/HvPap-10	大麦Hordeum vulgare L.	[63]
根的发育过程 Root development	AtCEP2	拟南芥Arabidopsis	[77]
花药绒毡层PCD过程 Programmed cell death of anther tapetum	CEP1	拟南芥Arabidopsis	[83]
	βVPE	拟南芥Arabidopsis	[84]

生长发育过程 Function	酶种类 Cysteine proteases	物种 Species	文献 Reference
叶衰老过程 Leaf senescence	SAG12	拟南芥Arabidopsis	[15]
	BnSAG12	油菜Napus	[19]
	NtSAG12	烟草Nicotiana tabacum L.	[21]
	OsSAG12-1	水稻Oryza sativa L.	[33]
	OsSAG12-2	水稻Oryza sativa L.	[34]
	HvPap-1/HvPap-19	大麦Hordeum vulgare L.	[18]
	HvPAP-14	大麦Hordeum vulgare L.	[37]
维管组织的PCD过程 Programmed cell death of vascular organization	ZCP4	百日草Zinnia	[40-41]
	AtXCP1/AtXCP2	拟南芥Arabidopsis	[46-47]
	γVPE	拟南芥Arabidopsis	[49-50,52]
种子萌发过程 Seed germination	EPA	大麦Hordeum vulgare L.	[58]
	EPB	大麦Hordeum vulgare L.	[53-54]
	HvPap-1	大麦Hordeum vulgare L.	[61-62]
	βVPE	拟南芥Arabidopsis	[48]
	δVPE	拟南芥Arabidopsis	[72]
	HvPap-4/HvPap-6/HvPap-10	大麦Hordeum vulgare L.	[63]
根的发育过程 Root development	AtCEP2	拟南芥Arabidopsis	[77]
花药绒毡层PCD过程 Programmed cell death of anther tapetum	CEP1	拟南芥Arabidopsis	[83]
	βVPE	拟南芥Arabidopsis	[84]