Research Progress on CFEM Proteins in Phytopathogenic Fungi

FU Xiuxia; LI Zhiyu; WU Yujia; LI Wei

doi:10.19303/j.issn.1008-0384.2022.012.015

Volume 37 Issue 12

Dec. 2022

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Article Navigation > Fujian Journal of Agricultural Sciences > 2022 > 37(12): 1626-1632

FU X X, LI Z Y, WU Y J, et al. Research Progress on CFEM Proteins in Phytopathogenic Fungi [J]. Fujian Journal of Agricultural Sciences，2022，37（12）：1626−1632 doi: 10.19303/j.issn.1008-0384.2022.012.015

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FU X X, LI Z Y, WU Y J, et al. Research Progress on CFEM Proteins in Phytopathogenic Fungi [J]. Fujian Journal of Agricultural Sciences，2022，37（12）：1626−1632 doi: 10.19303/j.issn.1008-0384.2022.012.015

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Research Progress on CFEM Proteins in Phytopathogenic Fungi

doi: 10.19303/j.issn.1008-0384.2022.012.015

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

Received Date: 2022-10-12
Accepted Date: 2022-10-12
Rev Recd Date: 2022-10-21

Available Online: 2022-12-28

Publish Date: 2022-03-28

Abstract

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

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References(56)

References

[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