植物病原真菌CFEM蛋白研究进展

付秀霞; 李志宇; 吴羽佳; 李魏

doi:10.19303/j.issn.1008-0384.2022.012.015

植物病原真菌CFEM蛋白研究进展

doi: 10.19303/j.issn.1008-0384.2022.012.015

1.
湖南农业大学植物保护学院，湖南　长沙　410128
2.
湖南省临湘市云湖街道农业综合服务中心，湖南　临湘　414300

基金项目: 杂交水稻国家重点实验室开放课题（2021KF05）；湖南省“揭榜挂帅”项目（2021NK1040）；湖南省自然科学基金项目（2021JJ30010）；湖南省研究生科研创新项目（2022XC066）

详细信息

作者简介:
付秀霞（1998−），女，硕士，研究方向：植物与病原物互作（E-mail：1943736689@qq.com）

通讯作者:
李魏（1983−），男，博士，教授，研究方向：植物与病原物互作（E-mail：liwei350551@163.com）

中图分类号: S 435
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- 被引次数: 0
出版历程
- 收稿日期: 2022-10-12
- 录用日期: 2022-10-12
- 修回日期: 2022-10-21
- 网络出版日期: 2022-12-28
- 刊出日期: 2022-03-28

Research Progress on CFEM Proteins in Phytopathogenic Fungi

FU Xiuxia^1
,,
LI Zhiyu²,
WU Yujia¹,
LI Wei^{1
, ,}

1.
College of Plant Protection, Hunan Agricultural University, Changsha, Hunan　410128, China
2.
Comprehensive Agricultural Service Center in Yunhu Street, Linxiang, Hunan　414300, China

摘要

摘要: 病原真菌在侵染植物过程中，往往分泌效应因子增加致病性或被寄主抗病基因识别激发寄主强烈抗性，因此效应因子在植物-病原物的互作中发挥重要作用。CFEM（Common in Fungal Extracellular Membrane）蛋白是真菌中特有的一类位于细胞外膜的蛋白，往往起效应因子的作用。本文综述了植物病原真菌CFEM蛋白家族的结构特点，在不同物种中的表达和定位，CFEM蛋白对真菌胞内铁吸收和生长发育方面的调控作用，抑制寄主免疫反应和促进真菌寄生的作用机制以及CFEM蛋白起源和进化过程等方面的研究进展，同时对目前CFEM蛋白研究有待阐明的问题进行了讨论并展望了未来的研究方向。本文将有助于人们进一步了解植物-病原真菌互作分子机理以及CFEM蛋白的致病机理，为培育作物抗病品种和制定植物真菌病害防控策略提供参考。
- 植物病原真菌 /
- CFEM蛋白 /
- 植物免疫 /
- 铁吸收
Abstract: In the process of infecting plants, pathogenic fungi may often secrete effectors to increase pathogenicity, or conversely, be recognized by the host to trigger resistance. Hence, such effectors are crucial for the well-being of a plant at time of a pathogenic intrusion. As an effector, CFEM (common in fungal extracellular membrane) protein is found only in the outer membrane of a fungal pathogen. This article reviews the origin, evolution, growth, development, structural characteristics, expressions and localization in different species, and intracellular iron absorption regulations of the CFEM protein family as well as the host immunology and infection-promoting factors associated with the proteins in the phytopathogens. Some of the yet-to-be-clarified issues on the molecular mechanisms and plant-pathogen interactions relating to CFEM proteins are discussed to facilitate the cultivation of disease-resistant plants and the development of ecologically friendly disease control strategies on crops.
- Phytopathogenic fungi /
- CFEM protein /
- plant immunity /
- iron absorption

HTML全文

图 1 CFEM结构域中高度保守的半胱氨酸

Figure 1. Highly conserved cysteines in CFEM protein domain

下载: 全尺寸图片幻灯片

图 2 白色念珠菌Csa2蛋白的CFEM结构

a：Csa2蛋白3个CFEM结构域的3D晶体结构为三聚体（引自NCBI）； b：Csa2蛋白的分子组分及它们之间相互作用示意图。A、B、C分别代表3个不同的CFEM结构域，1，2，3分别代表血红素B/C、氯离子和1,2-乙二醇。

Figure 2. Structure of CFEM protein domain in Csa2 of Candida albicans

a: “3D crystal structure of 3 CFEM protein domains in Csa2 is a trimer” as quoted from NCBI; b: Schematic molecular components and interactions of Csa2. A, B, and C represent 3 CFEM protein domains; 1, 2, and 3 represent heme B/C, chloride ion, and 1,2-ethanediol, respectively.

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参考文献(56)

[1]	SNELDERS N C, ROVENICH H, PETTI G C, et al. A plant pathogen utilizes effector proteins for microbiome manipulation [J]. Nature Plants, 2020(1): 926725.
[2]	LIU W D, LIU J L, TRIPLETT L, et al. Novel insights into rice innate immunity against bacterial and fungal pathogens [J]. Annual Review of Phytopathology, 2014, 52: 213−241. doi: 10.1146/annurev-phyto-102313-045926
[3]	TORUÑO T Y, STERGIOPOULOS I, COAKER G. Plant-pathogen effectors: Cellular probes interfering with plant defenses in spatial and temporal manners [J]. Annual Review of Phytopathology, 2016, 54: 419−441. doi: 10.1146/annurev-phyto-080615-100204
[4]	RAFIQI M, ELLIS J G, LUDOWICI V A, et al. Challenges and progress towards understanding the role of effectors in plant-fungal interactions [J]. Current Opinion in Plant Biology, 2012, 15(4): 477−482. doi: 10.1016/j.pbi.2012.05.003
[5]	XU Q, TANG C, WANG X, et al. An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function [J]. Nature Communications, 2019, 10(1): 5571. doi: 10.1038/s41467-019-13487-6
[6]	KULKARNI R D, KELKAR H S, DEAN R A. An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins [J]. Trends in Biochemical Sciences, 2003, 28(3): 118−121. doi: 10.1016/S0968-0004(03)00025-2
[7]	ZHANG Z N, WU Q Y, ZHANG G Z, et al. Systematic analyses reveal uniqueness and origin of the CFEM domain in fungi [J]. Scientific Reports, 2015, 5: 13032. doi: 10.1038/srep13032
[8]	YAKIR V, YANA S, EMMA L, et al. The three Aspergillus fumigatus CFEM-domain GPI-anchored proteins (CfmA-C) affect cell-wall stability but do not play a role in fungal virulence [J]. Fungal Genetics and Biology, 2014, 63: 55−64. doi: 10.1016/j.fgb.2013.12.005
[9]	RAMANUJAM R, CALVERT M E, SELVARAJ P, et al. The late endosomal hops complex anchors active g-protein signaling essential for pathogenesis in Magnaporthe oryzae [J]. PLoS Pathogens, 2013, 9(8): e1003527. doi: 10.1371/journal.ppat.1003527
[10]	WEISSMAN Z, KORNITZER D. A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization [J]. Molecular Microbiology, 2004, 53(4): 1209−1220. doi: 10.1111/j.1365-2958.2004.04199.x
[11]	KOU Y, TAN Y H, RAMANUJAM R, et al. Structure-function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast [J]. The New Phytologist, 2017, 214(1): 330−342. doi: 10.1111/nph.14347
[12]	GONG A D, JING Z Y, ZHANG K, et al. Bioinformatic analysis and functional characterization of the CFEM proteins in maize anthracnose fungus Colletotrichum graminicola [J]. Journal of Integrative Agriculture, 2020, 19(2): 541−550. doi: 10.1016/S2095-3119(19)62675-4
[13]	NASSER L, WEISSMAN Z, PINSKY M, et al. Structural basis of haem-iron acquisition by fungal pathogens [J]. Nat Microbiol, 2016, 1(11): 16156. doi: 10.1038/nmicrobiol.2016.156
[14]	ZHU W, WEI W, WU Y, et al. BcCFEM1, a CFEM domain-containing protein with putative GPI-anchored site, is involved in pathogenicity, conidial production, and stress tolerance in Botrytis cinerea [J]. Frontiers in Microbiology, 2017, 8: 1807. doi: 10.3389/fmicb.2017.01807
[15]	ARYA G C, SRIVASTAVA D A, PANDARANAYAKA E P J, et al. Characterization of the role of a non-GPCR membrane-bound CFEM protein in the pathogenicity and germination of Botrytis cinerea [J]. Microorganisms, 2020, 8(7): E1043. doi: 10.3390/microorganisms8071043
[16]	LING J, ZENG F, CAO Y X, et al. Identification of a class of CFEM proteins containing a new conserved motif in Fusarium oxysporum [J]. Physiological and Molecular Plant Pathology, 2015, 89: 41−48. doi: 10.1016/j.pmpp.2014.12.001
[17]	DING C, VIDANES G M, MAGUIRE S L, et al. Conserved and divergent roles of Bcr1 and CFEM proteins in Candida parapsilosis and Candida albicans [J]. PLoS One, 2011, 6(12): e28151. doi: 10.1371/journal.pone.0028151
[18]	CHEN C, PANDE K, FRENCH S D, et al. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis [J]. Cell Host & Microbe, 2011, 10(2): 118−135.
[19]	SORGO A G, BRUL S, DE KOSTER C G, et al. Iron restriction-induced adaptations in the wall proteome of Candida albicans[J]. Microbiology (Reading, England), 2013, 159(pt 8): 1673－1682.
[20]	SOSINSKA G J, DE KONING L J, DE GROOT P W J, et al. Mass spectrometric quantification of the adaptations in the wall proteome of Candida albicans in response to ambient pH[J]. Microbiology (Reading), 2011, 157(pt 1): 136－146.
[21]	PÉREZ A, RAMAGE G, BLANES R, et al. Some biological features of Candida albicans mutants for genes coding fungal proteins containing the CFEM domain [J]. FEMS Yeast Research, 2011, 11(3): 273−284. doi: 10.1111/j.1567-1364.2010.00714.x
[22]	PENG J, WU L, ZHANG W, et al. Systemic identification and functional characterization of common in fungal extracellular membrane proteins in Lasiodiplodia theobromae [J]. Front Plant Sci, 2021, 12: 804696. doi: 10.3389/fpls.2021.804696
[23]	井忠英. 玉米炭疽病菌CFEM效应子的系统鉴定与功能分析[D]. 北京: 中国农业科学院, 2015. JING Z Y. Systematic identification and functional analysis of CFEM effectors in Colletotrichum graminicola[D]. Beijing: Chinese Academy of Agricultural Sciences Dissertation, 2015. (in Chinese)
[24]	DENG J, DEAN R A. Characterization of adenylate cyclase interacting protein ACI1 in the rice blast fungus, Magnaporthe oryzae [J]. Open Mycology Journal, 2008, 2(1): 74−81. doi: 10.2174/1874437000802010074
[25]	DEZWAAN T M, CARROLL A M, VALENT B, et al. Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues [J]. Plastic and Reconstructive Surgery, 1999, 11(10): 2013−2030.
[26]	XU X, LI G, LI L, et al. Genome-wide comparative analysis of putative Pth11-related G protein-coupled receptors in fungi belonging to Pezizomycotina [J]. BMC Microbiology, 2017, 17(1): 166. doi: 10.1186/s12866-017-1076-5
[27]	CAI N, LIU R, YAN D, et al. Bioinformatics analysis and functional characterization of the CFEM proteins of Metarhizium anisopliae [J]. J Fungi (Basel), 2022, 8(7): 661. doi: 10.3390/jof8070661
[28]	WANG D, ZHANG D D, SONG J, et al. Verticillium dahliae CFEM proteins manipulate host immunity and differentially contribute to virulence [J]. BMC Biol, 2022, 20(1): 55. doi: 10.1186/s12915-022-01254-x
[29]	KULKARNI R D, THON M R, PAN H, et al. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea [J]. Genome Biol, 2005, 6(3): R24. doi: 10.1186/gb-2005-6-3-r24
[30]	张真娜. CFEM结构域在真菌中的进化研究[D]. 昆明: 云南大学, 2012. ZHANG Z N. Evolutionary pattems of CFEM domain in fungi[D]. Kunming: Yunnan university, 2012. (in Chinese)
[31]	JAMES T Y, KAUFF F, SCHOCH C L, et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny [J]. Nature, 2006, 443(7113): 818−822. doi: 10.1038/nature05110
[32]	MOUKADIRI I, ARMERO J, ABAD A, et al. Identification of a mannoprotein present in the inner layer of the cell wall of Saccharomyces cerevisiae [J]. RSC Advances, 1997, 179(7): 2154−2162.
[33]	INOKUMA K, KITADA Y, BAMBA T, et al. Improving the functionality of surface-engineered yeast cells by altering the cell wall morphology of the host strain [J]. Applied Microbiology and Biotechnology, 2021, 105(14/15): 5895−5904.
[34]	PENDLETON A L, SMITH K E, FEAU N, et al. Duplications and losses in gene families of rust pathogens highlight putative effectors [J]. Frontiers in Plant Science, 2014, 5: 299.
[35]	VELA-CORCÍA D, BAUTISTA R, DE VICENTE A, et al. De novo analysis of the epiphytic transcriptome of the cucurbit powdery mildew fungus Podosphaera xanthii and identification of candidate secreted effector proteins [J]. PLoS One, 2016, 11(10): e0163379. doi: 10.1371/journal.pone.0163379
[36]	XING Y, XU N, BHANDARI D D, et al. Bacterial effector targeting of a plant iron sensor facilitates iron acquisition and pathogen colonization [J]. The Plant Cell, 2021, 33(6): 2015−2031. doi: 10.1093/plcell/koab075
[37]	ALBAROUKI E, DEISING H B. Infection structure-specific reductive iron assimilation is required for cell wall integrity and full virulence of the maize pathogen Colletotrichum Graminicola [J]. Molecular Plant-Microbe Interactions, 2013, 26(6): 695−708. doi: 10.1094/MPMI-01-13-0003-R
[38]	KUZNETS G, VIGONSKY E, WEISSMAN Z, et al. A relay network of extracellular heme-binding proteins drives C. albicans iron acquisition from hemoglobin [J]. PLoS Pathogens, 2014, 10(10): e1004407. doi: 10.1371/journal.ppat.1004407
[39]	YE F, ALBAROUKI E, LINGAM B, et al. An adequate Fe nutritional status of maize suppresses infection and biotrophic growth of Colletotrichum Graminicola [J]. Physiologia Plantarum, 2014, 151(3): 280−292. doi: 10.1111/ppl.12166
[40]	OKAMOTO-SHIBAYAMA K, KIKUCHI Y, KOKUBU E, et al. Csa2, a member of the Rbt5 protein family, is involved in the utilization of iron from human hemoglobin during Candida albicans hyphal growth [J]. FEMS Yeast Research, 2014, 14(4): 674−677. doi: 10.1111/1567-1364.12160
[41]	SRIVASTAVA V K, SUNEETHA K J, KAUR R. A systematic analysis reveals an essential role for high-affinity iron uptake system, haemolysin and CFEM domain-containing protein in iron homoeostasis and virulence in Candida glabrata [J]. The Biochemical Journal, 2014, 463(1): 103−114. doi: 10.1042/BJ20140598
[42]	SABNAM N, ROY BARMAN S. WISH, a novel CFEM GPCR is indispensable for surface sensing, asexual and pathogenic differentiation in rice blast fungus [J]. Fungal Genetics and Biology, 2017, 105: 37−51. doi: 10.1016/j.fgb.2017.05.006
[43]	皮磊. 希金斯炭疽菌效应分子ChEP011和ChEP113的功能分析[D]. 广州: 华南农业大学, 2019. PI L. Functional analysis of effectors ChEP011 and ChEP113 of Colletotrichum higginsianum[D]. Guangzhou: South China Agricultural University, 2019. (in Chinese)
[44]	ELLIS J G, RAFIQI M, GAN P, et al. Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens [J]. Current Opinion in Plant Biology, 2009, 12(4): 399−405. doi: 10.1016/j.pbi.2009.05.004
[45]	GONG A D, JING Z Y, ZHANG K, et al. Bioinformatic analysis and functional characterization of the cfem proteins in maize anthracnose fungus Colletotrichum graminicola [J]. Journal of Integrative Agriculture, 2020(2): 541−550.
[46]	VÁZQUEZ-AVENDAÑO R, RODRÍGUEZ-HAAS J B, VELÁZQUEZ-DELGADO H, et al. Insights of the Neofusicoccum parvum-Liquidambar styraciflua interaction and identification of new cysteine-rich proteins in both species [J]. Journal of Fungi (Basel, Switzerland), 2021, 7(12): 1027.
[47]	CHEN L, WANG H, YANG J, et al. Bioinformatics and transcriptome analysis of CFEM proteins in Fusarium graminearum [J]. J Fungi (Basel), 2021, 7(10): 871. doi: 10.3390/jof7100871
[48]	ZHAO S, SHANG X, BI W, et al. Genome-wide identification of effector candidates with conserved motifs from the wheat leaf rust fungus Puccinia triticina [J]. Front Microbiol, 2020, 11: 1188. doi: 10.3389/fmicb.2020.01188
[49]	CHEN S, SONGKUMARN P, VENU R C, et al. Identification and characterization of in planta-expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice [J]. Mol Plant Microbe Interact, 2013, 26(2): 191−202. doi: 10.1094/MPMI-05-12-0117-R
[50]	GUO X, ZHONG D, XIE W, et al. Functional identification of novel cell death-inducing effector proteins from Magnaporthe oryzae [J]. Rice (New York, N Y ), 2019, 12(1): 59.
[51]	纪旭. 核盘菌分泌蛋白SsCFEM1的功能研究[D]. 长春: 吉林大学, 2020. JI X. Functional analysis of the secretory protein SsCFEM1 in Sclerotinia sclerotiorum[D]. Changchun: Jilin University, 2020. (in Chinese)
[52]	PENG Y J, HOU J, ZHANG H, et al. Systematic contributions of CFEM domain-containing proteins to iron acquisition are essential for inter species interaction of the filamentous pathogenic fungus Beauveria bassiana [J]. Environmental Microbiology, 2022, 24(8): 3693−3704. doi: 10.1111/1462-2920.16032
[53]	PÉREZ A, PEDRÓS B, MURGUI A, et al. Biofilm formation by Candida albicans mutants for genes coding fungal proteins exhibiting the eight-cysteine-containing CFEM domain [J]. FEMS Yeast Research, 2006, 6(7): 1074−1084. doi: 10.1111/j.1567-1364.2006.00131.x
[54]	CHOI W, DEAN R A. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development [J]. PLoS One, 1997, 9(11): 1973−1983.
[55]	SALOMON D, KINCH L N, TRUDGIAN D C, et al. Marker for type VI secretion system effectors [J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(25): 9271−9276. doi: 10.1073/pnas.1406110111
[56]	JIN Q C, DONG H T, PENG Y L, et al. Application of cDNA array for studying the gene expression profile of mature appressoria of Magnaporthe grisea [J]. J Zhejiang Univ Sci B, 2007, 8(2): 88−97. doi: 10.1631/jzus.2007.B0088