类钙调蛋白在植物生长发育及逆境胁迫中的功能研究进展
|
摘要
作为Ca~(2+)信号系统的重要家族成员,类钙调蛋白(CMLs)参与植物的各种生理生化过程,包括生长发育、生物胁迫、非生物胁迫和激素作用等。本文就类钙调蛋白在植物生长发育过程中功能的研究进展进行系统的综述,并对类钙调蛋白相关领域的研究进行展望,以期为CMLs的深入研究提供参考。
As an important family member of Ca~(2+) signal system, CMLs(calmodulin-like proteins) are involved in various physiological and biochemical processes of plants, including growth and development, biotic stress, abiotic stress, hormone action, etc. This paper reviews the CMLs function in the process of plant growth and development progress of research on systematic, and outlook the type of calmodulin related research, so as to provide reference for the further research of CMLs.
As an important family member of Ca~(2+) signal system, CMLs(calmodulin-like proteins) are involved in various physiological and biochemical processes of plants, including growth and development, biotic stress, abiotic stress, hormone action, etc. This paper reviews the CMLs function in the process of plant growth and development progress of research on systematic, and outlook the type of calmodulin related research, so as to provide reference for the further research of CMLs.
引文
Astegno A,Bonza MC,Vallone R,et al(2017).Arabidopsis calmodulin-like protein CML36 is a calcium(Ca2+)sensor that interacts with the plasma membrane Ca2+-ATPase isoform ACA8 and stimulates its activity.J Biol Chem,292:jbc.M117.787796
Bender KW,Dobney S,Ogunrinde A,et al(2014).The calmodulin-like protein CML43 functions as a salicylic-acid-inducible root specific Ca2+sensor in Arabidopsis.Biochem J,457(1):127-136
Bender KW,Snedden WA(2013).Calmodulin-related proteins step out from the shadow of their namesake.Plant Physiol,163(2):486-495
Bender KW,Rosenbaum DM,Vanderbeld B,et al(2013).The Arabidopsis calmodulin-like protein,CML39,functions during early seedling establishment.Plant J,76(4):634-647
Birhaou B(2008).The control of Arabidopsis thaliana flowering time by the calcium binding protein-22/Calmodulin-like 10 gene.Be’er Sheva,The State of Israel:Ben-Gurion University of the Negev
Boonburapong B,Buaboocha T(2007).Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins.BMC Plant Biol,7:4
Braam J,Davis RW(1990).Rain-,wind-,and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis.Cell,60(3):357-364
Campos WF,Dressano K,Ceciliato PHO,et al(2017).Arabidopsis thaliana rapid alkalinization factor 1-mediated root growth inhibition is dependent on calmodulin-like protein 38.J Biol Chem,293(6):2159-2171
Chehab EW,Yao C,Henderson Z,et al(2012).Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests.Curr Biol,22(8):701-706
Chen C,Duanmu HZ,Zhu D,et al(2015).Bioinformatics analysis of GMCML genes in soybean genome.Soybean Sci,34(6):957-963(in Chinese with English abstract).[陈超,端木慧子,朱丹等(2015).大豆CML家族基因的生物信息学分析.大豆科学,34(6):957-963]
Chen C,Sun XL,Duanmu HZ,et al(2015).GsCML27,a gene encoding a calcium binding ef-hand protein from Glycine soja,plays differential roles in plant responses to bicarbonate,salt and osmotic stresses.PLoS ONE,10(11):e0141888
Cheng HQ,Han LB,Yang CL,et al(2016).The cotton MYB108forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection.J Exp Bot,67(6):1935-1950
Chiasson D,Ekengren SK,Martin GB,et al(2005).Calmodulin-like proteins from Arabidopsis and tomato are involved in host defense against Pseudomonas syringae pv.tomato.Plant Mol Biol,58(6):887-897
Cho KM,Nguyen HT,Kim SY,et al(2016).CML10,a variant of calmodulin,modulates ascorbic acid synthesis.New Phytol,209(2):664-678
Cui SJ,Wang HH,Ma LG,et al(1998).The effects of extracellular of style and pollen on pollen germination and pollen tube growth.Acta Phytophysiol Sin,24(4):320-326(in Chinese with English abstract)[崔素娟,王洪梅,马力耕等(1998).花柱和花粉胞外钙调素对花粉萌发和花粉管伸长的影响.植物生理学报,24(4):320-326]
Delk NA,Johnson KA,Chowdhury NI,et al(2005).CML24,regulated in expression by diverse stimuli,encodes a potential sensor that ftmctions in responses to abscisic acid,daylength,and ion stress.Plant Physiol,139(1):240-253
Dobney S,Chiasson D,Lam P,et al(2009).The calmodulin-related calcium sensor CML42 plays a role in trichome branching.J Biol Chem,284(46):31647-31657
Dolze E,Chigri F,H?wing T,et al(2013).Calmodulin-like protein AtCML3 mediates dimerization of peroxisomal processing protease AtDEG 15 and contributes to normal peroxisome metabolism.Plant Mol Biol,83:607-624
Finkelstein RR,Gampala SS,Rock CD(2002).Abscisic acid signaling in seeds and seedlings.Plant Cell,14:S15-S45
He YH(2015).Expression analysis of calmodulin and calmodulin-like gene family and ionome analysis of cotton fiber(dissertation).Wuhan:Huazhong Agricultural University(in Chinese with English abstract)[何永辉(2015).棉花钙调素与类钙调素基因家族表达分析及棉花纤维离子组测定(学位论文).武汉:华中农业大学]
Hirai MY,Sawada Y,Kanaya S,et al(2010).Toward genome-wide metabolotyping and elucidation of metabolic system:metabolic profiling of large-scale bioresources.JPlant Res,123(3):291-298
Jung H,Chung PJ,Park SH,et al(2017).Overexpression of OsERF48 causes regulation of OsCML16,a calmodulin-like protein gene that enhances root growth and drought tolerance.Plant Biotechnol J,15(10):1295-1308
Leba LJ,Cheval C,Ortiz-Martín I,et al(2012).CML9,an Arabidopsis calmodulin-like protein,contributes to plant innate immunity through a flagellin-dependent signalling pathway.Plant J,71(6):976-989
Liang L,Flury S,Kalck V,et al(2006).CENTRIN2 interacts with the Arabidopsis homolog of the human XPC protein(AtRAD4)and contributes to efficient synthesis-dependent repair of bulky DNA lesions.Plant Mol Biol,61(1-2):345-356
Liao J,Deng J,Qin Z,et al(2017).Genome-wide identification and analyses of calmodulins and calmodulin-like proteins in Lotus japonicas.Front Plant Sci,8:482
Liu H,Deng Z,Chen JS,et al(2015).Cloning and expression analysis of calmodulin-like protein gene HbCML27from Hevea brasiliensis.Mol Plant Breeding,13(12):2721-2727(in Chinese with English abstract)[刘辉,邓治,陈江淑等(2015).巴西橡胶树类钙调素蛋白基因HbCML27克隆与表达分析.分子植物育种,13(12):2721-2727]
Ma W,Smigel A,Tsai YC,et al(2008).Innate immunity signaling:cytosolic Ca2+elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein.Plant Physiol,148(2):818-828
Magnan F,Ranty B,Charpenteau M,et al(2008).Mutations in AtCML9,a calmodulin-like protein from Arabidopsis thaliana,alter plant responses to abiotic stress and abscisic acid.Plant J,56(4):575-589
Mccormack E,Braam J(2003).Calmodulins and related potential calcium sensors of Arabidopsis.New Phytol,159:585-598
Mccormack E,Tsai YC,Braam J(2005).Handling calcium signaling:Arabidopsis CaMs and CMLs.Trends Plant Sci,10(8):383-389
Munir S,Liu H,Xing Y,et al(2016a).Overexpression of calmodulinlike(ShCML44)stress-responsive gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses.Sci Rep,6:31772
Munir S,Khan MR,Song J,et al(2016b).Genome-wide identification,characterization and expression analysis of calmodulin-like(CML)proteins in tomato(Solanum lycopersicum).Plant Physiol Biochem,102:167-179
Nakagami H,SoukupováH,Schikora A,et al(2006).A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis.J Biol Chem,281(50):38697-38704
Nakahara KS,Masuta C,Yamada S,et al(2012).Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors.Proc Natl Acad Sci USA,109(25):10113-10118
Nie SS,Zhang MJ,Zhang LG(2017).Genome-wide identification and expression analysis of calmodulin-like(CML)genes in Chinese cabbage(Brassica rapa L.ssp.pekinensis).BMC Genomics,18:842
Ogunrinde A,Munro K,Davidson A,et al(2017).Arabidopsis calmodulin-like proteins,CML15 and CML16 possess biochemical properties distinct from calmodulin and show non-overlapping tissue expression patterns.Front Plant Sci,8:2175
Park HC,Park CY,Koo SC,et al(2010).AtCML8,a calmodulin-like protein,differentially activating CaM-dependent enzymes in Arabidopsis thaliana.Plant Cell Rep,29(11):1297-1304
Popescu SC,Popescu GV,Bachan S,et al(2007).Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays.Proc Natl Acad Sci USA,104(11):4730-4735
Ruge H,Flosdorff S,Ebersberger I,et al(2016).The calmodulin-like proteins AtCML4 and AtCML5 are single-pass membrane proteins targeted to the endomembrane system by an N-terminal signal anchor sequence.J Exp Bot,67(13):3985-3996
Scholz SS,Vadassery J,Heyer M,et al(2014).Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory.Mol Plant,7(12):1712-1726
Teige M,Scheikl E,Eulgem T,et al(2004).The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis.Mol Cells,15(1):141-152
Trewavas A(2005).Green plants as intelligent organisms.Trends Plant Sci,10(9):413-419
Tsai YC,Delk NA,Chowdhury NI,et al(2007).Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering.Plant Signal Behav,2(6):446-454
Tsai YC,Koo Y,Delk NA,et al(2013).Calmodulin-related CML24 interacts with ATG4b and affects autophagy progression in Arabidopsis.Plant J,73(2):325-335
Vadassery J,Scholz SS,Mithofer A(2012a).Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived(Spodoptera littoralis)oral secretion.Plant Signal Behav,7(10):1277-1280
Vadassery J,Reichelt M,Hause B,et al(2012b).CML42-mediated calcium signaling coordinates responses to spodoptera herbivory and abiotic stresses in Arabidopsis.Plant Physiol,159(3):1159-1175
Vallone R,Verde VL,D’Onofrio M,et al(2016).Metal binding affinity and structural properties of calmodulin-like protein 14 from Arabidopsis thaliana.Protein Sci,25(8):1461-1471
Vanderbeld B,Snedden WA(2007).Developmental and stimulus-induced expression patterns of Arabidopsis calmodulin-like genes CML37,CML38 and CML39.Plant Mol Biol,64(6):683-697
Verslues PE,Zhu JK(2007).New developments in abscisic acid perception and metabolism.Curr Opin Plant Biol,10(5):447-452
Wang SS(2015).The study of CML25 regulating the pollen germination and pollen tube growth in Arabidopsis(dissertation).Jinan:Shandong University(in Chinese with English abstract).[王双双(2015).拟南芥CML25调控花粉萌发及花粉管生长的机理研究(学位论文).济南:山东大学]
Wang SS,Diao WZ,Yang X,et al(2015).Arabidopsis thaliana CML25 mediates the Ca2+regulation of K+transmembrane trafficking during pollen germination and tube elongation.Plant Cell Environ,38(11):2372-2386
Wang Y,Zhang WZ,Song LF,et al(2008).Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis.Plant Physiol,148(3):1201-1211
Wang YC(2011).Functions of CML24 in primary root mechanoresponses in Arabidopsis(dissertation).Chongqing:Chongqing University(in Chinese with English abstract).[王益川(2011).CML24在拟南芥主根机械响应中的作用(学位论文).重庆:重庆大学]
Wang YC,Wang BC,Simon GE,et al(2011).CML24 is involved in root mechanoresponses and cortical microtubule orientation in Arabidopsis.J Plant Growth Regul,30:467-479
Won SK,Lee YJ,Lee HY,et al(2009).Cis-element-and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis.Plant Physiol,150(3):1459-1473
Wu XM,Qiao Z,Liu HP,et al(2017).CML20,an Arabidopsis calmodulin-like protein,negatively regulates guard cell ABA signaling and drought stress tolerance.Front Plant Sci,8:824
Xu B,Cheval C,Laohavisit A,et al(2017).A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses.New Phytol,215(1):77
Xu GY,Rocha PS,Wang ML,et al(2011).A novel rice calmodulin-like gene,OsMSR2,enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis.Planta,234(1):47-59
Xu JQ(2014).Study of cloning and identification of calcium sensor protein-coding gene CML49 of pollen tube in Brassica oleracea L(dissertation).Chongqing:Southwest University(in Chinese with English abstract)[许俊强(2014).甘蓝花粉管钙感受蛋白编码基因CML49的克隆及功能鉴定研究(学位论文).重庆:西南大学]
Yamaguchi T,Aharon GS,Sottosanto JB,et al(2005).Vacuolar Na+/H+antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+-and p H-dependent manner.Proc Natl Acad Sci USA,102(44):16107-16112
Yang X(2014).Functional study of CML24 in regulating pollen germination and pollen tube growth(dissertation).Jinan:Shandong University(in Chinese with English abstract).[杨雪(2014).拟南芥CML24调控花粉萌发及花粉管生长的功能研究(学位论文).济南:山东大学]
Yang X,Wang SS,Wang M,et al(2014).Arabidopsis thaliana calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca2+concentration.Plant Mol Biol,86(3):225-236
Yin XM,Huang LF,Zhang X,et al(2015).OsCML4 improves drought tolerance through scavenging of reactive oxygen species in rice.J Plant Biol,58:68-73
Yu XJ,Cao SY,Dong YM,et al(2016).Research progress of calcium binding proteins in pollen growth and development.Acta Bot Boreali-Occident Sin,36(10):2121-2127(in Chinese with English abstract)[于晓俊,曹绍玉,董玉梅等(2016).钙结合蛋白对花粉生长发育调控研究进展.西北植物学报,36(10):2121-2127]
Zhao YX,Wei YL,Huang XZ(2014).Clone and expression analysis of calmodulin-like protein gene Op CML13 from olim Arabidopsis pumila of Xinjiang.Acta Bot Boreali-Occident Sin,34(3):431-437(in Chinese with English abstract).[赵云霞,魏艳玲,黄先忠(2014).新疆无苞芥类钙调素蛋白基因OPCML13的克隆与分析.西北植物学报,34(3):431-437]
Zhou L,Fu Y,Yang Z(2009).A genome-wide functional characterization of Arabidopsis regulatory calcium sensors in pollen tubes.J Integr Plant Biol,51(8):751-761
Zhu X,Robe E,Jomat L,et al(2017).CML8,an Arabidopsis calmodulin-like protein,plays a role in Pseudomonas syringae plant immunity.Plant Cell Physiol,58(2):307-319
Zipfel C,Felix G(2005).Plants and animals:a different taste for microbes?Curr Opin Plant Biol,8(4):353-360
Bender KW,Dobney S,Ogunrinde A,et al(2014).The calmodulin-like protein CML43 functions as a salicylic-acid-inducible root specific Ca2+sensor in Arabidopsis.Biochem J,457(1):127-136
Bender KW,Snedden WA(2013).Calmodulin-related proteins step out from the shadow of their namesake.Plant Physiol,163(2):486-495
Bender KW,Rosenbaum DM,Vanderbeld B,et al(2013).The Arabidopsis calmodulin-like protein,CML39,functions during early seedling establishment.Plant J,76(4):634-647
Birhaou B(2008).The control of Arabidopsis thaliana flowering time by the calcium binding protein-22/Calmodulin-like 10 gene.Be’er Sheva,The State of Israel:Ben-Gurion University of the Negev
Boonburapong B,Buaboocha T(2007).Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins.BMC Plant Biol,7:4
Braam J,Davis RW(1990).Rain-,wind-,and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis.Cell,60(3):357-364
Campos WF,Dressano K,Ceciliato PHO,et al(2017).Arabidopsis thaliana rapid alkalinization factor 1-mediated root growth inhibition is dependent on calmodulin-like protein 38.J Biol Chem,293(6):2159-2171
Chehab EW,Yao C,Henderson Z,et al(2012).Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests.Curr Biol,22(8):701-706
Chen C,Duanmu HZ,Zhu D,et al(2015).Bioinformatics analysis of GMCML genes in soybean genome.Soybean Sci,34(6):957-963(in Chinese with English abstract).[陈超,端木慧子,朱丹等(2015).大豆CML家族基因的生物信息学分析.大豆科学,34(6):957-963]
Chen C,Sun XL,Duanmu HZ,et al(2015).GsCML27,a gene encoding a calcium binding ef-hand protein from Glycine soja,plays differential roles in plant responses to bicarbonate,salt and osmotic stresses.PLoS ONE,10(11):e0141888
Cheng HQ,Han LB,Yang CL,et al(2016).The cotton MYB108forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection.J Exp Bot,67(6):1935-1950
Chiasson D,Ekengren SK,Martin GB,et al(2005).Calmodulin-like proteins from Arabidopsis and tomato are involved in host defense against Pseudomonas syringae pv.tomato.Plant Mol Biol,58(6):887-897
Cho KM,Nguyen HT,Kim SY,et al(2016).CML10,a variant of calmodulin,modulates ascorbic acid synthesis.New Phytol,209(2):664-678
Cui SJ,Wang HH,Ma LG,et al(1998).The effects of extracellular of style and pollen on pollen germination and pollen tube growth.Acta Phytophysiol Sin,24(4):320-326(in Chinese with English abstract)[崔素娟,王洪梅,马力耕等(1998).花柱和花粉胞外钙调素对花粉萌发和花粉管伸长的影响.植物生理学报,24(4):320-326]
Delk NA,Johnson KA,Chowdhury NI,et al(2005).CML24,regulated in expression by diverse stimuli,encodes a potential sensor that ftmctions in responses to abscisic acid,daylength,and ion stress.Plant Physiol,139(1):240-253
Dobney S,Chiasson D,Lam P,et al(2009).The calmodulin-related calcium sensor CML42 plays a role in trichome branching.J Biol Chem,284(46):31647-31657
Dolze E,Chigri F,H?wing T,et al(2013).Calmodulin-like protein AtCML3 mediates dimerization of peroxisomal processing protease AtDEG 15 and contributes to normal peroxisome metabolism.Plant Mol Biol,83:607-624
Finkelstein RR,Gampala SS,Rock CD(2002).Abscisic acid signaling in seeds and seedlings.Plant Cell,14:S15-S45
He YH(2015).Expression analysis of calmodulin and calmodulin-like gene family and ionome analysis of cotton fiber(dissertation).Wuhan:Huazhong Agricultural University(in Chinese with English abstract)[何永辉(2015).棉花钙调素与类钙调素基因家族表达分析及棉花纤维离子组测定(学位论文).武汉:华中农业大学]
Hirai MY,Sawada Y,Kanaya S,et al(2010).Toward genome-wide metabolotyping and elucidation of metabolic system:metabolic profiling of large-scale bioresources.JPlant Res,123(3):291-298
Jung H,Chung PJ,Park SH,et al(2017).Overexpression of OsERF48 causes regulation of OsCML16,a calmodulin-like protein gene that enhances root growth and drought tolerance.Plant Biotechnol J,15(10):1295-1308
Leba LJ,Cheval C,Ortiz-Martín I,et al(2012).CML9,an Arabidopsis calmodulin-like protein,contributes to plant innate immunity through a flagellin-dependent signalling pathway.Plant J,71(6):976-989
Liang L,Flury S,Kalck V,et al(2006).CENTRIN2 interacts with the Arabidopsis homolog of the human XPC protein(AtRAD4)and contributes to efficient synthesis-dependent repair of bulky DNA lesions.Plant Mol Biol,61(1-2):345-356
Liao J,Deng J,Qin Z,et al(2017).Genome-wide identification and analyses of calmodulins and calmodulin-like proteins in Lotus japonicas.Front Plant Sci,8:482
Liu H,Deng Z,Chen JS,et al(2015).Cloning and expression analysis of calmodulin-like protein gene HbCML27from Hevea brasiliensis.Mol Plant Breeding,13(12):2721-2727(in Chinese with English abstract)[刘辉,邓治,陈江淑等(2015).巴西橡胶树类钙调素蛋白基因HbCML27克隆与表达分析.分子植物育种,13(12):2721-2727]
Ma W,Smigel A,Tsai YC,et al(2008).Innate immunity signaling:cytosolic Ca2+elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein.Plant Physiol,148(2):818-828
Magnan F,Ranty B,Charpenteau M,et al(2008).Mutations in AtCML9,a calmodulin-like protein from Arabidopsis thaliana,alter plant responses to abiotic stress and abscisic acid.Plant J,56(4):575-589
Mccormack E,Braam J(2003).Calmodulins and related potential calcium sensors of Arabidopsis.New Phytol,159:585-598
Mccormack E,Tsai YC,Braam J(2005).Handling calcium signaling:Arabidopsis CaMs and CMLs.Trends Plant Sci,10(8):383-389
Munir S,Liu H,Xing Y,et al(2016a).Overexpression of calmodulinlike(ShCML44)stress-responsive gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses.Sci Rep,6:31772
Munir S,Khan MR,Song J,et al(2016b).Genome-wide identification,characterization and expression analysis of calmodulin-like(CML)proteins in tomato(Solanum lycopersicum).Plant Physiol Biochem,102:167-179
Nakagami H,SoukupováH,Schikora A,et al(2006).A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis.J Biol Chem,281(50):38697-38704
Nakahara KS,Masuta C,Yamada S,et al(2012).Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors.Proc Natl Acad Sci USA,109(25):10113-10118
Nie SS,Zhang MJ,Zhang LG(2017).Genome-wide identification and expression analysis of calmodulin-like(CML)genes in Chinese cabbage(Brassica rapa L.ssp.pekinensis).BMC Genomics,18:842
Ogunrinde A,Munro K,Davidson A,et al(2017).Arabidopsis calmodulin-like proteins,CML15 and CML16 possess biochemical properties distinct from calmodulin and show non-overlapping tissue expression patterns.Front Plant Sci,8:2175
Park HC,Park CY,Koo SC,et al(2010).AtCML8,a calmodulin-like protein,differentially activating CaM-dependent enzymes in Arabidopsis thaliana.Plant Cell Rep,29(11):1297-1304
Popescu SC,Popescu GV,Bachan S,et al(2007).Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays.Proc Natl Acad Sci USA,104(11):4730-4735
Ruge H,Flosdorff S,Ebersberger I,et al(2016).The calmodulin-like proteins AtCML4 and AtCML5 are single-pass membrane proteins targeted to the endomembrane system by an N-terminal signal anchor sequence.J Exp Bot,67(13):3985-3996
Scholz SS,Vadassery J,Heyer M,et al(2014).Mutation of the Arabidopsis calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to herbivory.Mol Plant,7(12):1712-1726
Teige M,Scheikl E,Eulgem T,et al(2004).The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis.Mol Cells,15(1):141-152
Trewavas A(2005).Green plants as intelligent organisms.Trends Plant Sci,10(9):413-419
Tsai YC,Delk NA,Chowdhury NI,et al(2007).Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering.Plant Signal Behav,2(6):446-454
Tsai YC,Koo Y,Delk NA,et al(2013).Calmodulin-related CML24 interacts with ATG4b and affects autophagy progression in Arabidopsis.Plant J,73(2):325-335
Vadassery J,Scholz SS,Mithofer A(2012a).Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived(Spodoptera littoralis)oral secretion.Plant Signal Behav,7(10):1277-1280
Vadassery J,Reichelt M,Hause B,et al(2012b).CML42-mediated calcium signaling coordinates responses to spodoptera herbivory and abiotic stresses in Arabidopsis.Plant Physiol,159(3):1159-1175
Vallone R,Verde VL,D’Onofrio M,et al(2016).Metal binding affinity and structural properties of calmodulin-like protein 14 from Arabidopsis thaliana.Protein Sci,25(8):1461-1471
Vanderbeld B,Snedden WA(2007).Developmental and stimulus-induced expression patterns of Arabidopsis calmodulin-like genes CML37,CML38 and CML39.Plant Mol Biol,64(6):683-697
Verslues PE,Zhu JK(2007).New developments in abscisic acid perception and metabolism.Curr Opin Plant Biol,10(5):447-452
Wang SS(2015).The study of CML25 regulating the pollen germination and pollen tube growth in Arabidopsis(dissertation).Jinan:Shandong University(in Chinese with English abstract).[王双双(2015).拟南芥CML25调控花粉萌发及花粉管生长的机理研究(学位论文).济南:山东大学]
Wang SS,Diao WZ,Yang X,et al(2015).Arabidopsis thaliana CML25 mediates the Ca2+regulation of K+transmembrane trafficking during pollen germination and tube elongation.Plant Cell Environ,38(11):2372-2386
Wang Y,Zhang WZ,Song LF,et al(2008).Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis.Plant Physiol,148(3):1201-1211
Wang YC(2011).Functions of CML24 in primary root mechanoresponses in Arabidopsis(dissertation).Chongqing:Chongqing University(in Chinese with English abstract).[王益川(2011).CML24在拟南芥主根机械响应中的作用(学位论文).重庆:重庆大学]
Wang YC,Wang BC,Simon GE,et al(2011).CML24 is involved in root mechanoresponses and cortical microtubule orientation in Arabidopsis.J Plant Growth Regul,30:467-479
Won SK,Lee YJ,Lee HY,et al(2009).Cis-element-and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis.Plant Physiol,150(3):1459-1473
Wu XM,Qiao Z,Liu HP,et al(2017).CML20,an Arabidopsis calmodulin-like protein,negatively regulates guard cell ABA signaling and drought stress tolerance.Front Plant Sci,8:824
Xu B,Cheval C,Laohavisit A,et al(2017).A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses.New Phytol,215(1):77
Xu GY,Rocha PS,Wang ML,et al(2011).A novel rice calmodulin-like gene,OsMSR2,enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis.Planta,234(1):47-59
Xu JQ(2014).Study of cloning and identification of calcium sensor protein-coding gene CML49 of pollen tube in Brassica oleracea L(dissertation).Chongqing:Southwest University(in Chinese with English abstract)[许俊强(2014).甘蓝花粉管钙感受蛋白编码基因CML49的克隆及功能鉴定研究(学位论文).重庆:西南大学]
Yamaguchi T,Aharon GS,Sottosanto JB,et al(2005).Vacuolar Na+/H+antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+-and p H-dependent manner.Proc Natl Acad Sci USA,102(44):16107-16112
Yang X(2014).Functional study of CML24 in regulating pollen germination and pollen tube growth(dissertation).Jinan:Shandong University(in Chinese with English abstract).[杨雪(2014).拟南芥CML24调控花粉萌发及花粉管生长的功能研究(学位论文).济南:山东大学]
Yang X,Wang SS,Wang M,et al(2014).Arabidopsis thaliana calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca2+concentration.Plant Mol Biol,86(3):225-236
Yin XM,Huang LF,Zhang X,et al(2015).OsCML4 improves drought tolerance through scavenging of reactive oxygen species in rice.J Plant Biol,58:68-73
Yu XJ,Cao SY,Dong YM,et al(2016).Research progress of calcium binding proteins in pollen growth and development.Acta Bot Boreali-Occident Sin,36(10):2121-2127(in Chinese with English abstract)[于晓俊,曹绍玉,董玉梅等(2016).钙结合蛋白对花粉生长发育调控研究进展.西北植物学报,36(10):2121-2127]
Zhao YX,Wei YL,Huang XZ(2014).Clone and expression analysis of calmodulin-like protein gene Op CML13 from olim Arabidopsis pumila of Xinjiang.Acta Bot Boreali-Occident Sin,34(3):431-437(in Chinese with English abstract).[赵云霞,魏艳玲,黄先忠(2014).新疆无苞芥类钙调素蛋白基因OPCML13的克隆与分析.西北植物学报,34(3):431-437]
Zhou L,Fu Y,Yang Z(2009).A genome-wide functional characterization of Arabidopsis regulatory calcium sensors in pollen tubes.J Integr Plant Biol,51(8):751-761
Zhu X,Robe E,Jomat L,et al(2017).CML8,an Arabidopsis calmodulin-like protein,plays a role in Pseudomonas syringae plant immunity.Plant Cell Physiol,58(2):307-319
Zipfel C,Felix G(2005).Plants and animals:a different taste for microbes?Curr Opin Plant Biol,8(4):353-360