TAL Effectors with Avirulence Activity in African Strains of Xanthomonas oryzae pv. oryzae
Tóm tắt
Xanthomonas oryzae pv. oryzae (Xoo) causes bacterial leaf blight, a devastating disease of rice. Among the type-3 effectors secreted by Xoo to support pathogen virulence, the Transcription Activator-Like Effector (TALE) family plays a critical role. Some TALEs are major virulence factors that activate susceptibility (S) genes, overexpression of which contributes to disease development. Host incompatibility can result from TALE-induced expression of so-called executor (E) genes leading to a strong and rapid resistance response that blocks disease development. In that context, the TALE functions as an avirulence (Avr) factor. To date no such avirulence factors have been identified in African strains of Xoo. With respect to the importance of TALEs in the Rice-Xoo pathosystem, we aimed at identifying those that may act as Avr factor within African Xoo. We screened 86 rice accessions, and identified 12 that were resistant to two African strains while being susceptible to a well-studied Asian strain. In a gain of function approach based on the introduction of each of the nine tal genes of the avirulent African strain MAI1 into the virulent Asian strain PXO99A, four were found to trigger resistance on specific rice accessions. Loss-of-function mutational analysis further demonstrated the avr activity of two of them, talD and talI, on the rice varieties IR64 and CT13432 respectively. Further analysis of TalI demonstrated the requirement of its activation domain for triggering resistance in CT13432. Resistance in 9 of the 12 rice accessions that were resistant against African Xoo specifically, including CT13432, could be suppressed or largely suppressed by trans-expression of the truncTALE tal2h, similarly to resistance conferred by the Xa1 gene which recognizes TALEs generally independently of their activation domain. We identified and characterized TalD and TalI as two African Xoo TALEs with avirulence activity on IR64 and CT13432 respectively. Resistance of CT13432 against African Xoo results from the combination of two mechanisms, one relying on the TalI-mediated induction of an unknown executor gene and the other on an Xa1-like gene or allele.
Tài liệu tham khảo
Ainsworth EA (2008) Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Glob Chang Biol 14:1642–1650. https://doi.org/10.1111/j.1365-2486.2008.01594.x
Boch J, Scholze H, Schornack S et al (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science (80-) 326:1509–1512. https://doi.org/10.1126/science.1178811
Boch J, Bonas U, Lahaye T (2014) TAL effectors—pathogen strategies and plant resistance engineering. New Phytol 204:823–832. https://doi.org/10.1111/nph.13015
Cernadas RA, Doyle EL, Niño-Liu DO et al (2014) Code-assisted discovery of TAL effector targets in bacterial leaf streak of rice reveals contrast with bacterial blight and a novel susceptibility gene. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1003972
Chen X, Liu P, Mei L et al (2021) Xa7, a new executor R gene that confers durable and broad-spectrum resistance to bacterial blight disease in rice. Plant Commun 2:100143. https://doi.org/10.1016/j.xplc.2021.100143
Chu Z, Fu B, Yang H et al (2006) Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor Appl Genet 112:455–461. https://doi.org/10.1007/s00122-005-0145-6
Djedatin G, Ndjiondjop MN, Mathieu T et al (2011) Evaluation of African cultivated rice Oryza glaberrima for resistance to bacterial blight. Plant Dis 95:441–447. https://doi.org/10.1094/PDIS-08-10-0558
Doucouré H, Pérez-Quintero AL, Reshetnyak G et al (2018) Functional and genome sequence-driven characterization of tal effector gene repertoires reveals novel variants with altered specificities in closely related malian Xanthomonas oryzae pv. oryzae strains. Front Microbiol 9:1–17. https://doi.org/10.3389/fmicb.2018.01657
Doyle EL, Booher NJ, Standage DS et al (2012) TAL effector-nucleotide targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res 40:W117–W122. https://doi.org/10.1093/nar/gks608
Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci 76:1648–1652. https://doi.org/10.1073/PNAS.76.4.1648
Fragoso CA, Moreno M, Wang Z, et al (2017) Genetic architecture of a rice nested association mapping population. G3 Genes|Genomes|Genetics 7:1913–1926. https://doi.org/10.1534/G3.117.041608
Garcia-Ruiz H, Szurek B, Van den Ackerveken G (2021) Stop helping pathogens: engineering plant susceptibility genes for durable resistance. Curr Opin Biotechnol 70:187–195. https://doi.org/10.1016/j.copbio.2021.05.005
Gonzalez C, Szurek B, Manceau C et al (2007) Molecular and pathotypic characterization of new Xanthomonas oryzae strains from West Africa. Mol Plant-Microbe Interact 20:534–546. https://doi.org/10.1094/MPMI-20-5-0534
Gu K, Yang B, Tian D et al (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125. https://doi.org/10.1038/nature03630
Hopkins C, White F, Choi S et al (1992) Identification of a Family of Avirulence Genes from Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 5:451–459. https://doi.org/10.1094/MPMI-5-451
Hu K, Cao J, Zhang J et al (2017) Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat Plants. https://doi.org/10.1038/nplants.2017.9
Hutin M, Sabot F, Ghesquière A et al (2015) A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J 84:694–703. https://doi.org/10.1111/tpj.13042
Ji Z, Ji C, Liu B et al (2016) Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat Commun 7:1–9. https://doi.org/10.1038/ncomms13435
Ji C, Ji Z, Liu B et al (2020) Xa1 allelic R genes activate rice blight resistance suppressed by interfering TAL effectors. Plant Commun 1:100087. https://doi.org/10.1016/j.xplc.2020.100087
Jiang N, Yan J, Liang Y et al (2020) Resistance genes and their interactions with bacterial blight/leaf streak pathogens (Xanthomonas oryzae) in rice (Oryza sativa L.)—an updated review. Rice. https://doi.org/10.1186/s12284-019-0358-y
Lang JM, Pérez-Quintero AL, Koebnik R et al (2019) A pathovar of Xanthomonas oryzae infecting wild grasses provides insight into the evolution of pathogenicity in rice agroecosystems. Front Plant Sci 10:507. https://doi.org/10.3389/fpls.2019.00507
Liu Q, Yuan M, Zhou Y et al (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ 34:1958–1969. https://doi.org/10.1111/J.1365-3040.2011.02391.X
Liu W, Liu J, Triplett L et al (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu Rev Phytopathol 52:213–241. https://doi.org/10.1146/annurev-phyto-102313-045926
Luo D, Huguet-Tapia JC, Raborn RT et al (2021) The Xa7 resistance gene guards the rice susceptibility gene SWEET14 against exploitation by the bacterial blight pathogen. Plant Commun 2:100164. https://doi.org/10.1016/j.xplc.2021.100164
Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science (80-) 326:1501. https://doi.org/10.1126/science.1178817
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326. https://doi.org/10.1093/NAR/8.19.4321
Niño-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324. https://doi.org/10.1111/j.1364-3703.2006.00344.x
Oliva R, Ji C, Atienza-Grande G et al (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol 37:1344–1350. https://doi.org/10.1038/s41587-019-0267-z
Pérez-Quintero AL, Rodriguez-R LM, Dereeper A et al (2013) An improved method for TAL effectors DNA-binding sites prediction reveals functional convergence in TAL repertoires of Xanthomonas oryzae Strains. PLoS ONE. https://doi.org/10.1371/journal.pone.0068464
Poulin L, Grygiel P, Magne M et al (2015) New multilocus variable-number tandem-repeat analysis tool for surveillance and local epidemiology of bacterial leaf blight and bacterial leaf streak of rice caused by Xanthomonas oryzae. Appl Environ Microbiol 81:688–698. https://doi.org/10.1128/AEM.02768-14
Read AC, Rinaldi FC, Hutin M et al (2016) Suppression of Xo1-mediated disease resistance in rice by a truncated, non-DNA-binding TAL effector of Xanthomonas oryzae. Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.01516
Read AC, Hutin M, Moscou MJ et al (2020a) Cloning of the rice Xo1 resistance gene and interaction of the Xo1 protein with the defense-suppressing Xanthomonas effector Tal2h. Mol Plant-Microbe Interact 33:1189–1195. https://doi.org/10.1094/MPMI-05-20-0131-SC
Read AC, Moscou MJ, Zimin A V et al (2020b) Genome assembly and characterization of a complex zfBED-NLR genecontaining disease resistance locus in Carolina Gold Select rice with Nanopore sequencing. PLOS Genet 16:e1008571. https://doi.org/10.1371/journal.pgen.1008571
Ryba-White M, Notteghem JL, Leach J (1995) Comparison of Xanthomonas oryzae pv. oryzae strains from Africa, North America, and Asia by restriction fragment length polymorphism analysis. https://agris.fao.org/agris-search/search.do?recordID=QR9500053. Accessed 14 Aug 2021
Savary S, Willocquet L, Pethybridge SJ et al (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439. https://doi.org/10.1038/s41559-018-0793-y
Schandry N, Jacobs JM, Szurek B, Perez-Quintero AL (2018) A cautionary TALE: how plant breeding may have favoured expanded TALE repertoires in Xanthomonas. Mol Plant Pathol 19:1297. https://doi.org/10.1111/MPP.12670
Song W-YY, Wang G-LL, Chen L-LL et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science (80-) 270:1804. https://doi.org/10.1126/science.270.5243.1804
Strauss T, Van Poecke RMP, Strauß A et al (2012) RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large-crop genome. Proc Natl Acad Sci U S A 109:19480–19485. https://doi.org/10.1073/pnas.1212415109
Streubel J, Pesce C, Hutin M et al (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819. https://doi.org/10.1111/nph.12411
Sun X, Cao Y, Yang Z et al (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527. https://doi.org/10.1046/j.1365-313X.2003.01976.x
Tekete C, Cunnac S, Doucouré H et al (2020) Characterization of new races of Xanthomonas oryzae pv. oryzae in mali informs resistance gene deployment. Phytopathology 110:267–277. https://doi.org/10.1094/PHYTO-02-19-0070-R
Tharreau D, Notteghem JL, Morel JB, et al (2007) Developing Blast Durable Resistance By Using The Wild Rice Species, Oryza rufipogon : Presentasi RUTI IV. http://perpus.biotek.lipi.go.id/perpus/index.php?p=show_detail&id=15794&keywords=
Tian D, Wang J, Zeng X et al (2014) The Rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 26:497–515. https://doi.org/10.1105/tpc.113.119255
Tran TT, Pérez-Quintero AL, Wonni I et al (2018) Functional analysis of African Xanthomonas oryzae pv. oryzae TALomes reveals a new susceptibility gene in bacterial leaf blight of rice. PLoS Pathog 14:1–25. https://doi.org/10.1371/journal.ppat.1007092
Triplett LR, Hamilton JP, Buell CR et al (2011) Genomic analysis of Xanthomonas oryzae isolates from rice grown in the united states reveals substantial divergence from known X. oryzae pathovars. Appl Environ Microbiol 77:3930–3937. https://doi.org/10.1128/AEM.00028-11
Triplett LR, Cohen SP, Heffelfinger C et al (2016) A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant J 87:472–483. https://doi.org/10.1111/tpj.13212
Utami DW, Barnita K, Yuriah S, Hanarida I (2011) Nucleotide base variation of blast disease resistance gene Pi33 in rice selected broad genetic background. HAYATI J Biosci 18:123–128. https://doi.org/10.4308/hjb.18.3.123
Wang C, Qin TF, Yu HM et al (2014) The broad bacterial blight resistance of rice line CBB23 is triggered by a novel transcription activator-like (TAL) effector of Xanthomonas oryzae pv. oryzae. Mol Plant Pathol 15:333–341. https://doi.org/10.1111/mpp.12092
Wang C, Zhang X, Fan Y et al (2015) XA23 Is an executor r protein and confers broad-spectrum disease resistance in rice. Mol Plant 8:290–302. https://doi.org/10.1016/j.molp.2014.10.010
Wonni I, Hutin M, Ouédrago L et al (2016) Evaluation of elite rice varieties unmasks new sources of bacterial blight and leaf streak resistance for Africa. Rice Res Open Access 4:1–8. https://doi.org/10.4172/2375-4338.1000162
Xiang Y, Cao Y, Xu C et al (2006) Xa3, conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein, is the same as Xa26. Theor Appl Genet 113:1347–1355. https://doi.org/10.1007/s00122-006-0388-x
Yu Y, Streubel J, Balzergue S et al (2011) Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol Plant-Microbe Interact 24:1102–1113. https://doi.org/10.1094/MPMI-11-10-0254
Zhang J, Yin Z, White F (2015) TAL effectors and the executor R genes. Front Plant Sci 6:1–9. https://doi.org/10.3389/fpls.2015.00641
Zhang B, Zhang H, Li F, et al (2020) Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to Xanthomonas oryzae pv. oryzae. Plant Commun 1:100088. https://doi.org/10.1016/j.xplc.2020.100088