摘要
Mildew resistance locus O(MLO)蛋白是植物特有的一类蛋白家族,其中的部分成员是白粉病菌成功侵染寄主植物的必要因子。一个或多个MLO基因的功能缺失突变可赋予植物对白粉病菌广谱且持久的抗性,mlo介导的白粉病抗性在抗病育种中发挥了重要作用。植物中的MLO蛋白可以分为7个亚家族,除了参与植物与白粉病菌的互作外,不同亚家族的MLO蛋白还有很多其他功能。本文对MLO蛋白的特征、分类、功能进行了归纳,介绍了植物与白粉病抗性相关的mlo突变体特征及抗病机制,并对MLO基因的功能、作用机理研究及其在植物抗病育种中利用应注意的问题进行了讨论。
Mildew resistance locus O(MLO) is a plant-specific protein family, some of which are essential factors for the powdery mildew successfully infection. Loss-of-function mutation of one or more MLO genes can confer the host plants durable broad-spectrum resistance to powdery mildew. mlo-based resistance has been successfully employed in plant resistance breeding. Plant MLO proteins can be divided into 7 subfamilies. In addition to the plant-powdery mildew interaction, MLOs from different subfamilies may have different functions. This review introduces the characteristic, categorization and function of MLO proteins, as well as the features and possible resistance mechanisms of mlo mutant. At last, we discuss the function mechanism of MLO proteins, the utilization of MLO genes in the plant disease resistance breeding and the problems we should pay attention to.
引文
Ablazov A,Tombuloglu H(2015).Genome-wide identification of the mildew resistance locus O(MLO)gene family in novel cereal model species Brachypodium distachyon.Eur J Plant Pathol,145(2):239-253
Acevedo-Garcia J,Gruner K,Reinst?dler A,et al(2017).The powdery mildew-resistant Arabidopsis mlo2 mlo6 mlo12triple mutant displays altered infection phenotypes with diverse types of phytopathogens.Sci Rep,7(1):9319
Acevedo-Garcia J,Kusch S,Panstruga R(2014).Magical mystery tour:MLO proteins in plant immunity and beyond.New Phytol,204(2):273-281
Acevedo-Garcia J,Spencer D,Thieron H,et al(2017).mlobased powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach.Plant Biotechnol J,15(3):367-378
Appiano M,Pavan S,Catalano D,et al(2015).Identification of candidate MLO powdery mildew susceptibility genes in cultivated Solanaceae and functional characterization of tobacco Nt MLO1.Transgenic Res,24(5):847-858
Bai Y,Pavan S,Zheng Z,et al(2008).Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of Mlo function.Mol Plant Microbe Interact,21(1):30-39
Bayles CJ,Aist JR(1987).Apparent calcium mediation of resistance of an ml-o barley mutant to powdery mildew.Physiol Mol Plant Pathol,30:337-345
Berg JA,Appiano M,Bijsterbosch G(2017).Functional characterization of cucumber(Cucumis sativus L.)Clade VMLO genes.BMC Plant Biol,17:80
Berg JA,Appiano M,Martínez MS,et al(2015).A transposable element insertion in the susceptibility gene Csa M-LO8 results in hypocotyl resistance to powdery mildew in cucumber.BMC Plant Biol,15:243
Bhat RA,Miklis M,Schmelzer E,et al(2005).Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain.Proc Natl Acad Sci USA,102(8):3135-3140
Bidzinski P,Noir S,Shahi S,et al(2014).Physiological characterization and genetic modifiers of aberrant root thigmomorphogenesis in mutants of Arabidopsis thaliana MILDEW LOCUS O genes.Plant Cell Environ,37:2738-2753
Blume B,Nürnberger T,Nass N,et al(2000).Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley.Plant Cell,12(8):1425-1440
Bockaert J,Pin JP(1999).Molecular tinkering of G protein-coupled receptors:an evolutionary success.EMBO J,18(7):1723-1729
Bombarely A,Rosli HG,Vrebalov J,et al(2012).A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research.Mol Plant Microbe Interact,25:1523-1530
Bracuto V,Appiano M,Ricciardi L,et al(2017).Functional characterization of the powdery mildew susceptibility gene Sm MLO1 in eggplant(Solanum melongena L.).Transgenic Res,26(3):323-330
Brzostowski JA,Kimmel AR(2001).Signaling at zero G:G-protein-independent functions for 7-TM receptors.Trends Biochem Sci,26(5):291-297
Büschges R,Hollricher K,Panstruga R,et al(1997).The barley Mlo gene:a novel control element of plant pathogen resistance.Cell,88:695-705
Chandran D,Inada N,Hather G,et al(2010).Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators.Proc Natl Acad Sci USA,107:460-465
Chen Y,Wang Y,Zhang H(2014).Genome-wide analysis of the mildew resistance locus(MLO)gene family in tomato(Solanum lycopersicum L.).Plant Omics J,7:87-93
Chen Z,Hartmann HA,Wu MJ,et al(2006).Expression analysis of the At MLO gene family encoding plant-specific seven-transmembrane domain proteins.Plant Mol Biol,60:583-597
Chen Z,Noir S,Kwaaitaal M,et al(2009).Two seven-transmembrane domain MILDEW RESISTANCE LOCUS Oproteins cofunction in Arabidopsis root thigmomorphogenesis.Plant Cell,21:1972-1991
Collins NC,Thordal-Christensen H,Lipka V,et al(2003).SNARE-protein-mediated disease resistance at the plant cell wall.Nature,425(6961):973-977
Consonni C,Bednarek P,Humphry M,et al(2010).Tryptophan-derived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant.Plant Physiol,152:1544-1561
Consonni C,Humphry ME,Hartmann HA,et al(2006).Conserved requirement for a plant host cell protein in powdery mildew pathogenesis.Nat Genet,38:716-720
Davis TC,Jones DS,Dino AJ,et al(2017).Arabidopsis thaliana MLO genes are expressed in discrete domains during reproductive development.Plant Reprod,30(4):185-195
Deshmukh R,Singh VK,Singh BD(2014).Comparative phylogenetic analysis of genome-wide Mlo gene family members from Glycine max and Arabidopsis thaliana.Mol Genet Genomics,289:345-359
Deshmukh R,Singh VK,Singh BD(2016).Comparative analysis of genome-wide Mlo gene family in Cajanus cajan and Phaseolus vulgaris.Genetica,144(2):229-241
Deshmukh R,Singh VK,Singh BD(2017).Mining the Cicer arietinum genome for the mildew locus O(Mlo)gene family and comparative evolutionary analysis of the Mlo genes from Medicago truncatula and some other plant species.J Plant Res,130(2):239-253
Devoto A,Hartmann HA,Piffanelli P,et al(2003).Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family.J Mol Evol,56:77-88
Devoto A,Piffanelli P,Nilsson IM,et al(1999).Topology,subcellular localization,and sequence diversity of the Mlo family in plants.J Biol Chem,274:34993-35004
Dong X,Zhao Y,Ran X,et al(2017).Overexpression of a new chitinase gene Eu CHIT2 enhances resistance to Erysiphe cichoracearum DC.in tobacco plants.Int J Mol Sci,18(11):2361-2366
Elliott C,Müller J,Miklis M,et al(2005).Conserved extracellular cysteine residues and cytoplasmic loop-loop interplay are required for functionality of the heptahelica MLO protein.Biochem J,385:243-254
Feechan A,Jermakow AM,Torregrosa L,et al(2008).Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew.Funct Plant Biol,35(12):1255-1266
Freisleben R,Lein A(1942).über die Auffindung einer mehltauresistenten Mutante nach R?ntgenbestrahlung einer anf?lligen reinen Linie von Sommergerste.Naturwissenschaften,30(40):608
Fujimura T,Sato S,Tajima T,et al(2016).Powdery mildew resistance in the Japanese domestic tobacco cultivar Kokubu is associated with aberrant splicing of MLO orthologues.Plant Pathol,65:1358-1365
Harland SC(1948).Inheritance of immunity to mildew in Peruvian forms of Pisum sativum.Heredity,2:263-269
Hofer K,Linkmeyer A,Textor K,et al(2015).MILDEWLOCUS O mutation does not affect resistance to grain infections with Fusarium spp.and Ramularia collo-cygni.Phytopathology,105:1214-1219
Howlader J,Park JI,Kim HT,et al(2017).Differential expression under Podosphaera xanthii and abiotic stresses reveals candidate MLO family genes in Cucumis melo L.Trop Plant Biol,10(4):151-168
Hückelhoven R,Dechert C,Kogel KH(2003).Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis.Proc Natl Acad Sci USA,100(9):5555-5560
Humphry M,Bednarek P,Kemmerling B,et al(2010).Aregulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity.Proc Natl Acad Sci USA,107(50):1896-1901
Humphry M,Reinst?dler A,Ivanov S,et al(2011).Durable broad-spectrum powdery mildew resistance in pea er1plants is conferred by natural loss-of-function mutations in Ps MLO1.Mol Plant Pathol,12:866-878
International Barley Genome Sequencing Consortium(2012).A physical,genetic and functional sequence assembly of the barley genome.Nature,491:711-716
Iovieno P,Andolfo G,Schiavulli A,et al(2015).Structure,evolution and functional inference on the Mildew Locus O(MLO)gene family in three cultivated Cucurbitaceae spp.BMC Genomics,16:1112
Jarosch B,Kogel KH,Schaffrath U(1999).The ambivalence of the barley Mlo locus:mutations conferring resistance against powdery mildew(Blumeria graminis f.sp.hordei)enhance susceptibility to the rice blast fungus Magnaporthe grisea.Mol Plant Microbe Interact,12:508-514
Jiang P,Chen Y,Wilde HD(2016).Reduction of MLO1 expression in petunia increases resistance to powdery mildew.Sci Hortic,201:225-229
Jiwan D,Roalson EH,Main D,et al(2013).Antisense expression of peach mildew resistance locus O(Pp Mlo1)gene confers cross-species resistance to powdery mildew in Fragaria×ananassa.Transgenic Res,22:1119-1131
Jones DS,Yuan J,Smith BE,et al(2017).MILDEW RESIS-TANCE LOCUS O function in pollen tube reception is linked to its oligomerization and subcellular distribution.Plant Physiol,175:172-185
J?rgensen JH(1992).Discovery,characterization and exploitation of Mlo powdery mildew resistance in barley.Euphytica,63:141-152
Kessler SA,Shimosato-Asano H,Keinath NF,et al(2010).Conserved molecular components for pollen tube reception and fungal invasion.Science,330:968-971
Kim DS,Hwang BK(2012).The pepper MLO gene,Ca M-LO2,is involved in the susceptibility cell-death response and bacterial and oomycete proliferation.Plant J,72:843-855
Kim MC,Lee SH,Kim JK,et al(2002a).Mlo,a modulator of plant defense and cell death,is a novel calmodulin-binding protein.Isolation and characterization of a rice Mlo homologue.J Biol Chem,277:19304-19314
Kim MC,Panstruga R,Elliott C,et al(2002b).Calmodulin interacts with MLO protein to regulate defence against mildew in barley.Nature,416:447-451
Koga H,Mayama S,Shishiyama J(1980).Correlation between the deposition of fluorescent compounds in papillae and resistance in barley against Erysiphe gratnitzis hordei.Can J Bot,58:536-541
Konishi S,Sasakuma T,Sasanuma T(2010).Identification of novel Mlo family members in wheat and their genetic characterization.Genes Genet Syst,85:167-175
Kuhn H,Lorek J,Kwaaitaal M,et al(2017).Key components of different plant defense pathways are dispensable for powdery mildew resistance of the Arabidopsis mlo2 mlo6mlo12 triple mutant.Front Plant Sci,8:1006
Kusch S,Panstruga R(2017).mlo-based resistance:an apparently universal“weapon”to defeat powdery mildew disease.Mol Plant Microbe Interact,30(3):179-189
Kusch S,Pesch L,Panstruga R(2016).Comprehensive phylogenetic analysis sheds light on the diversity and origin of the MLO family of integral membrane proteins.Genome Biol Evol,8(3):878-895
Lim CW,Lee SC(2013).Functional roles of the pepper MLOprotein gene,Ca MLO2,in abscisic acid signaling and drought sensitivity.Plant Mol Biol,85:1-10
Liu Q,Zhu H(2008).Molecular evolution of the MLO gene family in Oryza sativa and their functional divergence.Gene,409:1-10
Lorek J,Griebel T,Jones AM,et al(2013).The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity.Mol Plant Microbe Interact,26(9):991-1003
Lyngkj?r MF,Carver TLW(2000).Conditioning of cellular defence responses to powdery mildew in cereal leaves by prior attack.Mol Plant Pathol,1(1):41-49
Nekrasov V,Wang C,Win J,et al(2017).Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion.Sci Rep,7:482
Nguyen VNT,Vo KTX,Park H,et al(2016).A systematic view of the MLO family in rice suggests their novel roles in morphological development,diurnal responses,the light-signaling pathway,and various stress responses.Front Plant Sci,7:1413
Panstruga R(2005).Serpentine plant MLO proteins as entry portals for powdery mildew fungi.Biochem Soc Trans,33:389-392
Panstruga R,Schulze-Lefert P(2003).Corruption of host seven-transmembrane proteins by pathogenic microbes:a common theme in animals and plants?Microbes Infect,5:429-437
Pavan S,Schiavulli A,Appiano M,et al(2011).Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus.Theor Appl Genet,123:1425-1431
Pessina S,Angeli D,Martens S,et al(2016).The knock-down of the expression of Md MLO19 reduces susceptibility to powdery mildew(Podosphaera leucotricha)in apple(Malus domestica).Plant Biotechnol J,14(10):2033-2044
Pessina S,Palmieri L,Bianco L,et al(2017).Frequency of a natural truncated allele of Md MLO19 in the germplasm of Malus domestica.Mol Breeding,37:7
Pessina S,Pavan S,Catalano D,et al(2014).Characterization of the MLO gene family in Rosaceae and gene expression analysis in Malus domestica.BMC Genomics,15:618
Piffanelli P,Zhou F,Casais C,et al(2002).The barley MLOmodulator of defense and cell death is responsive to biotic and abiotic stress stimuli.Plant Physiol,129(3):1076-1085
Poovaiah BW,Du L,Wang H,et al(2013).Recent advances in calcium/calmodulin-mediated signaling with an emphasis on plant-microbe interactions.Plant Physiol,163(2):531-542
Qin B,Wang M,Liu Q,et al(2014).Identification and sequence characterization of Mlo gene family from the genome of Riciuns communis L.Chin Agr Sci Bull,30(15):268-273(in Chinese with English abstract)[覃碧,王萌,刘巧玲等(2014).蓖麻基因组Mlo基因家族成员的鉴定及其序列特征分析.中国农学通报,30(15):268-273]
Qin B,Wang M,Liu QL,et al(2013).Identification and sequence characterization of Mlo gene family from the genome of Manihot esculenta Crantz.Plant Physiol J,49(10):1057-1062(in Chinese with English abstract)[覃碧,王萌,刘巧玲等(2013).木薯Mlo基因家族成员的鉴定及其序列特征分析.植物生理学报,49(10):1057-1062]
Qiu X,Wang Q,Zhang H,et al(2015).Antisense Rh MLO1gene transformation enhances resistance to the powdery mildew pathogen in Rosa multiflora.Plant Mol Biol Rep,33:1659-1665
Riaz S,Boursiquot JM,Dangl GS,et al(2013).Identification of mildew resistance in wild and cultivated central Asian grape germplasm.BMC Plant Biol,13:149
Shen QH,Saijo Y,Mauch S,et al(2007).Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.Science,315:1098-1103
Skou JP(1982).Callose formation responsible for the powdery mildew resistance in barley with genes in the ml-o locus.J Phytopathol,104(1):90-95
Skou JP,J?rgensen JH,Lilholt U(1984).Comparative studies on callose formation in powdery mildew compatible and incompatible barley.Phytopath Z,109(2):147-168
Stein M,Dittgen J,Sánchez-Rodríguez C,et al(2006).Arabidopsis PEN3/PDR8,an ATP binding cassette transporter,contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration.Plant Cell,18(3):731-746
Stein M,Somerville S(2002).MLO,a novel modulator of plant defenses and cell death,binds calmodulin.Trends Plant Sci,7(9):379-380
Stolzenburg MC,Aist JR,Israel HW(1984).The role of papillae in resistance to powdery mildew conditioned by the ml-o gene in barley.I.Correlative evidence.Physiol Plant Pathol,25:337-346
Sun S,Deng D,Wang Z,et al(2016a).A novel er1 allele and the development and validation of its functional marker for breeding pea(Pisum sativum L.)resistance to powdery mildew.Theor Appl Genet,129:909-919
Sun S,Fu H,Wang Z,et al(2016b).Discovery of a novel er1 allele conferring powdery mildew resistance in Chinese pea(Pisum sativum L.)landraces.PLo S ONE,11:e0147624
Tang D,Christiansen KM,Innes RW(2005).Regulation of plant disease resistance,stress responses,cell death,and ethylene signaling in Arabidopsis by the EDR1 protein kinase.Plant Physiol,138:1018-1026
Temple BRS,Jones AM(2007).The plant heterotrimeric G-protein complex.Annu Rev Plant Biol,58:249-266
Underwood W,Somerville SC(2008).Focal accumulation of defences at sites of fungal pathogen attack.J Exp Bot,59(13):3501-3508
Vogel JP,Somerville S(2000).Isolation and characterization of powdery mildew-resistant Arabidopsis mutants.Proc Natl Acad Sci USA,97:1897-1902
Wang X,Ma Q,Dou L,et al(2016).Genome-wide characterization and comparative analysis of the MLO gene family in cotton.Plant Physiol Biochem,103:106-119
Wang Y,Cheng X,Shan Q,et al(2014).Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew.Nat Biotechnol,32(9):947-952
Wolter M,Hollricher K,Salamini F,et al(1993).The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype.Mol Gen Genet,239:122-128
Xiao S,Calis O,Patrick E,et al(2005).The atypical resistance gene,RPW8,recruits components of basal defence for powdery mildew resistance in Arabidopsis.Plant J,42:95-110
Xu H,Heath MC(1998).Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus.Plant Cell,10(4):585-597
Yan PZ,Zhou S,Li XH,et al(2017).Genome-wide comparative analysis of MLO related genes in Brassica lineage.Chin J Oil Crop Sci,39(6):729-736(in Chinese with English abstract)[闫沛喆,周索,李雪辉等(2017).全基因组水平上芸薹属Mlo抗病基因的比较分析.中国油料作物学报,39(6):729-736]
Yang T,Poovaiah BW(2003).Calcium/calmodulin-mediated signal network in plants.Trends Plant Sci,8(10):505-512
Yi J,An S,An G(2014).Os MLO12,encoding seven transmembrane proteins,is involved with pollen hydration in rice.Plant Reprod,27:169-180
Yuan P,Jauregui E,Du L,et al(2017).Calcium signatures and signaling events orchestrate plant-microbe interactions.Curr Opin Plant Biol,38:173-183
Zheng Z,Appiano M,Pavan S,et al(2016).Genome-wide study of the tomato Sl MLO gene family and its functional characterization in response to the powdery mildew fungus Oidium neolycopersici.Front Plant Sci,7:380
Zheng Z,Nonomura T,Appiano M,et al(2013).Loss of function in Mlo orthologs reduces susceptibility of pepper and tomato to powdery mildew disease caused by Leveillula taurica.PLo S ONE,8(7):e70723
Zhou SJ,Jing Z,Shi JL(2013).Genome-wide identification,characterization,and expression analysis of the MLOgene family in Cucumis sativus.Genet Mol Res,12:6565-6578
Zou S,Wang H,Li Y,et al(2018).The NB-LRR gene Pm60confers powdery mildew resistance in wheat.New Phytol,218:298-309