Rapid evolution in plant-microbe interactions - a molecular genomics perspective.
adaptation
dispensable chromosome
genome evolution
phytopathogens
virulence factors
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
08
03
2019
accepted:
14
05
2019
pubmed:
28
5
2019
medline:
17
12
2020
entrez:
29
5
2019
Statut:
ppublish
Résumé
Rapid (co-)evolution at multiple timescales is a hallmark of plant-microbe interactions. The mechanistic basis for the rapid evolution largely rests on the features of the genomes of the interacting partners involved. Here, we review recent insights into genomic characteristics and mechanisms that enable rapid evolution of both plants and phytopathogens. These comprise fresh insights in allelic series of matching pairs of resistance and avirulence genes, the generation of novel pathogen effectors, the recently recognised small RNA warfare, and genomic aspects of secondary metabolite biosynthesis. In addition, we discuss the putative contributions of permissive host environments, transcriptional plasticity and the role of ploidy on the interactions. We conclude that the means underlying the rapid evolution of plant-microbe interactions are multifaceted and depend on the particular nature of each interaction.
Substances chimiques
RNA, Plant
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1134-1142Informations de copyright
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.
Références
Azmi NSA, Singkaravanit-Ogawa S, Ikeda K, Kitakura S, Inoue Y, Narusaka Y, Shirasu K, Kaido M, Mise K, Takano Y. 2018. Inappropriate expression of an NLP effector in Colletotrichum orbiculare impairs infection on cucurbitaceae vultivars via plant recognition of the C-terminal region. Molecular Plant-Microbe Interactions 31: 101-111.
Belhaj K, Cano LM, Prince DC, Kemen A, Yoshida K, Dagdas YF, Etherington GJ, Schoonbeek H-J, van Esse HP, Jones JDG et al. 2016. Arabidopsis late blight: infection of a nonhost plant by Albugo laibachii enables full colonization by Phytophthora infestans. Cellular Microbiology 19: e12628.
Bódi Z, Farkas Z, Nevozhay D, Kalapis D, Lázár V, Csörgő B, Nyerges Á, Szamecz B, Fekete G, Papp B et al. 2017. Phenotypic heterogeneity promotes adaptive evolution. PLoS Biology 15: e2000644.
Borrelli GM, Mazzucotelli E, Marone D, Crosatti C, Michelotti V, Valè G, Mastrangelo AM. 2018. Regulation and evolution of NLR genes: a close interconnection for plant immunity. International Journal of Molecular Sciences 19: 1662.
Cai Q, Qiao L, Wang M, He B, Lin F-M, Palmquist J, Huang H-D, Jin H. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360: 1126-1129.
Cairns T, Meyer V. 2017. In silico prediction and characterization of secondary metabolite biosynthetic gene clusters in the wheat pathogen Zymoseptoria tritici. BMC Genomics 18: 631.
Carvunis A-R, Rolland T, Wapinski I, Calderwood MA, Yildirim MA, Simonis N, Charloteaux B, Hidalgo CA, Barbette J, Santhanam B et al. 2012. Proto-genes and de novo gene birth. Nature 487: 370-374.
Cesari S. 2018. Multiple strategies for pathogen perception by plant immune receptors. New Phytologist 219: 17-24.
Chujo T, Lukito Y, Eaton CJ, Dupont P-Y, Johnson LJ, Winter D, Cox MP, Scott B. 2019. Complex epigenetic regulation of alkaloid biosynthesis and host interaction by heterochromatin protein I in a fungal endophyte-plant symbiosis. Fungal Genetics & Biology 125: 71-83.
Courville KJ, Frantzeskakis L, Gul S, Haeger N, Kellner R, Heßler N, Day B, Usadel B, Gupta YK, van Esse HP et al. 2019. Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors. New Phytologist 222: 1474-1492.
van Dam P, Fokkens L, Ayukawa Y, van der Gragt M, Ter Horst A, Brankovics B, Houterman PM, Arie T, Rep M. 2017. A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species. Scientific Reports 7: 9042.
Davis MP, Carrieri C, Saini HK, van Dongen S, Leonardi T, Bussotti G, Monahan JM, Auchynnikava T, Bitetti A, Rappsilber J et al. 2017. Transposon-driven transcription is a conserved feature of vertebrate spermatogenesis and transcript evolution. EMBO Reports 18: 1231-1247.
Depotter JR, Seidl MF, Wood TA, Thomma BP. 2016. Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Current Opinion in Microbiology 32: 7-13.
Dong S, Raffaele S, Kamoun S. 2015. The two-speed genomes of filamentous pathogens: waltz with plants. Current Opinion in Plant Biology 35: 57-65.
Fiorin GL, Sanchéz-Vallet A, Thomazella DPdT, do Prado PFV, do Nascimento LC, Figueira AVdO, Thomma BPHJ, Pereira GAG, Teixeira PJPL. 2018. Suppression of plant immunity by fungal chitinase-like effectors. Current Biology 28: 3023.e5-3030.e5.
Fletcher K, Gil J, Bertier LD, Kenefick A, Wood KJ, Zhang L, Reyes-Chin-Wo S, Cavanaugh K, Tsuchida C, Wong J et al. 2019. Genomic signatures of heterokaryosis in the oomycete pathogen, Bremia lactucae. Nature Communications 10: 2645.
Fouché S, Plissonneau C, Croll D. 2018. The birth and death of effectors in rapidly evolving filamentous pathogen genomes. Current Opinion in Microbiology 46: 34-42.
Frantzeskakis L, Kusch S, Panstruga R. 2019. The need for speed: compartmentalized genome evolution in filamentous phytopathogens. Molecular Plant Pathology 20: 3-7.
Frantzeskakis L, von Dahlen JK, Panstruga R, Rose LE. 2018. Rapid evolution in the tug-of-war between microbes and plants. New Phytologist 219: 12-14.
Friesen TL, Stukenbrock EH, Liu ZH, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38: 953-956.
Hartmann FE, Croll D. 2017. Distinct trajectories of massive recent gene gains and losses in populations of a microbial eukaryotic pathogen. Molecular Biology and Evolution 34: 2808-2822.
Hartmann FE, Sánchez-Vallet A, McDonald BA, Croll D. 2017. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. ISME Journal 11: 1189-1204.
Hodgins-Davis A, Townsend JP. 2009. Evolving gene expression: from G to E to GxE. Trends in Ecology & Evolution 24: 649-658.
Hua C, Zhao J-H, Guo H-S. 2018. Trans-kingdom RNA silencing in plant-fungal pathogen interactions. Molecular Plant 11: 235-244.
Hurni S, Brunner S, Buchmann G, Herren G, Jordan T, Krukowski P, Wicker T, Yahiaoui N, Mago R, Keller B. 2013. Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. The Plant Journal 76: 957-969.
Inoue Y, Vy TTP, Yoshida K, Asano H, Mitsuoka C, Asuke S, Anh VL, Cumagun CJR, Chuma I, Terauchi R et al. 2017. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357: 80-83.
Kaiser CA, Preuss D, Grisafi P, Botstein D. 1987. Many random sequences functionally replace the secretion signal sequence of yeast invertase. Science 235: 312-317.
Karasov TL, Almario J, Friedemann C, Ding W, Giolai M, Heavens D, Kersten S, Lundberg DS, Neumann M, Regalado J et al. 2018. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associations over evolutionary timescales. Cell Host & Microbe 24: 168.e4-179.e4.
Kema GHJ, Gohari AM, Aouini L, Gibriel HAY, Ware SB, van den Bosch F, Manning-Smith R, Alonso-Chavez V, Helps J, M'Barek SB et al. 2018. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nature Genetics 50: 375.
Kessler D, Sang H, Bousquet A, Hulvey JP, Garcia D, Rhee S, Hoshino Y, Yamada T, Jung G. 2018. Nucleic adaptability of heterokaryons to fungicides in a multinucleate fungus, Sclerotinia homoeocarpa. Fungal Genetics & Biology 115: 64-77.
Kettle AJ, Batley J, Benfield AH, Manners JM, Kazan K, Gardiner DM. 2015. Degradation of the benzoxazolinone class of phytoalexins is important for virulence of Fusarium pseudograminearum towards wheat. Molecular Plant Pathology 16: 946-962.
Krishnan P, Ma X, McDonald BA, Brunner PC. 2018. Widespread signatures of selection for secreted peptidases in a fungal plant pathogen. BMC Evolutionary Biology 18: 7.
Kronstad JW, Leong SA. 1989. Isolation of two alleles of the b locus of Ustilago maydis. Proceedings of the National Academy of Sciences, USA 86: 978-982.
Lei Y, Wang M, Wan A, Xia C, See DR, Zhang M, Chen X. 2017. Virulence and molecular characterization of experimental isolates of the stripe rust pathogen (Puccinia striiformis) indicate somatic recombination. Phytopathology 107: 329-344.
Li Y, Shen H, Zhou Q, Qian K, van der Lee Theo, Huang S. 2017. Changing ploidy as a strategy: the Irish potato famine pathogen shifts ploidy in relation to its sexuality. Molecular Plant-Microbe Interactions 30: 45-52.
Lilley CJ, Maqbool A, Wu D, Yusup HB, Jones LM, Birch PRJ, Banfield MJ, Urwin PE, Eves-van den Akker S. 2018. Effector gene birth in plant parasitic nematodes: neofunctionalization of a housekeeping glutathione synthetase gene. PLoS Genetics 14: e1007310.
Lu X, Kracher B, Saur IML, Bauer S, Ellwood SR, Wise R, Yaeno T, Maekawa T, Schulze-Lefert P. 2016. Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proceedings of the National Academy of Sciences, USA 113: E6486-E6495.
Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
McDonald BA, Stukenbrock EH. 2016. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 371: 20160026.
McNally KE, Menardo F, Lüthi L, Praz CR, Müller MC, Kunz L, Ben-David R, Chandrasekhar K, Dinoor A, Cowger C et al. 2018. Distinct domains of the AVRPM3A2/F2 avirulence protein from wheat powdery mildew are involved in immune receptor recognition and putative effector function. New Phytologist 218: 681-695.
Meile L, Croll D, Brunner PC, Plissonneau C, Hartmann FE, McDonald BA, Sánchez-Vallet A. 2018. A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch. New Phytologist 219: 1048-1061.
Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S et al. 2016. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nature Genetics 48: 201-205.
Nelson RR. 1963. Interspecific hybridization in the fungi. Mycologia 55: 104-123.
Nottensteiner M, Zechmann B, McCollum C, Hückelhoven R. 2018. A barley powdery mildew fungus non-autonomous retrotransposon encodes a peptide that supports penetration success on barley. Journal of Experimental Botany 69: 3745-3758.
Palma-Guerrero J, Ma X, Torriani SFF, Zala M, Francisco CS, Hartmann FE, Croll D, McDonald BA. 2017. Comparative transcriptome analyses in Zymoseptoria tritici reveal significant differences in gene expression among strains during plant infection. Molecular Plant-Microbe Interactions 30: 231-244.
Palmer JM, Keller NP. 2010. Secondary metabolism in fungi: does chromosomal location matter? Current Opinion in Microbiology 13: 431-436.
Pennington HG, Jones R, Kwon S, Bonciani G, Thieron H, Chandler T, Luong P, Morgan SN, Przydacz M, Bozkurt T et al. 2019. The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathogens 15: e1007620.
Piasecka A, Jedrzejczak-Rey N, Bednarek P. 2015. Secondary metabolites in plant innate immunity. Conserved function of divergent chemicals. New Phytologist 206: 948-964.
Plissonneau C, Benevenuto J, Mohd-Assaad N, Fouché S, Hartmann FE, Croll D. 2017a. Using population and comparative genomics to understand the genetic basis of effector-driven fungal pathogen evolution. Frontiers in Plant Science 8: 119.
Plissonneau C, Blaise F, Ollivier B, Leflon M, Carpezat J, Rouxel T, Balesdent M-H. 2017b. Unusual evolutionary mechanisms to escape effector-triggered immunity in the fungal phytopathogen Leptosphaeria maculans. Molecular Ecology 26: 2183-2198.
Prats E, Carver Timothy LW, Lyngkjaer MF, Roberts PC, Zeyen RJ. 2006. Induced inaccessibility and accessibility in the oat powdery mildew system: insights gained from use of metabolic inhibitors and silicon nutrition. Molecular Plant Pathology 7: 47-59.
Praz CR, Bourras S, Zeng F, Sánchez-Martín J, Menardo F, Xue M, Yang L, Roffler S, Böni R, Herren G et al. 2017. AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytologist 213: 1301-1314.
Praz CR, Menardo F, Robinson MD, Müller MC, Wicker T, Bourras S, Keller B. 2018. Non-parent of origin expression of numerous effector genes indicates a role of gene regulation in host adaption of the hybrid triticale powdery mildew pathogen. Frontiers in Plant Science 9: 49.
Qutob D, Chapman BP, Gijzen M. 2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nature Communications 4: 1349.
Reynolds HT, Slot JC, Divon HH, Lysøe E, Proctor RH, Brown DW. 2017. Differential retention of gene functions in a secondary metabolite cluster. Molecular Biology and Evolution 34: 2002-2015.
Roca MG, Read ND, Wheals AE. 2005. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiology Letters 249: 191-198.
Rose LE, Overdijk EJR, van Damme M. 2019. Small RNA molecules and their role in plant disease. European Journal of Plant Pathology 153: 1-14.
Rouxel T, Balesdent M-H. 2017. Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. New Phytologist 214: 526-532.
Rufián JS, Macho AP, Corry DS, Mansfield JW, Ruiz-Albert J, Arnold DL, Beuzón CR. 2018. Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains. Molecular Plant Pathology 19: 537-551.
Saur IM, Bauer S, Kracher B, Lu X, Franzeskakis L, Müller MC, Sabelleck B, Kümmel F, Panstruga R, Maekawa T et al. 2019. Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife 8: e44471.
Schierstaedt J, Bziuk N, Kuzmanović N, Blau K, Smalla K, Jechalke S. 2019. Role of plasmids in plant-bacteria interactions. Current Issues in Molecular Biology 30: 17-38.
Schulze-Lefert P, Panstruga R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science 16: 117-125.
Seeholzer S, Tsuchimatsu T, Jordan T, Bieri S, Pajonk S, Yang WX, Jahoor A, Shimizu KK, Keller B, Schulze-Lefert P. 2010. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Molecular Plant-Microbe Interactions 23: 497-509.
Sperschneider J, Dodds PN, Gardiner DM, Singh KB, Taylor JM. 2018. Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Molecular Plant Pathology 19: 2094-2110.
Srichumpa P, Brunner S, Keller B, Yahiaoui N. 2005. Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiology 139: 885-895.
Thynne E, Mead O, Chooi Y-H, McDonald M, Solomon PS. 2019. Acquisition and loss of secondary metabolites shaped the evolutionary path of three emerging phytopathogens of wheat. Genome Biology and Evolution 11: 890-905.
Upson JL, Zess EK, Białas A, Wu C-H, Kamoun S. 2018. The coming of age of EvoMPMI: evolutionary molecular plant-microbe interactions across multiple timescales. Current Opinion in Plant Biology 44: 108-116.
Wei FS, Wong RA, Wise RP. 2002. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 14: 1903-1917.
Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342: 118-123.
Wu J, Kou Y, Bao J, Li Y, Tang M, Zhu X, Ponaya A, Xiao G, Li J, Li C et al. 2015. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytologist 206: 1463-1475.
Yomtovian I, Teerakulkittipong N, Lee B, Moult J, Unger R. 2010. Composition bias and the origin of ORFan genes. Bioinformatics 26: 996-999.
Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J et al. 2013. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2: e00731.
Zhang S, Wang L, Wu W, He L, Yang X, Pan Q. 2015. Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Scientific Reports 5: 11642.
Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C, Zala M, Ducasse A, Confais J, Compain J, Lapalu N et al. 2017. A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytologist 214: 619-631.