Analysis of three types of resistance gene analogs in PmU region from Triticum urartu

doi:10.1016/S2095-3119(18)61995-1

摘要/Abstract

Abstract: Resistance gene analog (RGA) screening of mapped disease-resistant genes not only helps to clone these genes but also helps to develop efficient molecular markers for resistance breeding. The present study focused on the PmU region located on chromosome 7A^uL of Triticum urartu, and recently, a nucleotide binding site (NBS)-encoding gene, Pm60, was cloned from the same chromosome arm. In this research, NBS, protein kinase (PK), and ATP-binding cassette (ABC), the three disease resistance-related gene families, were analyzed within PmU region by using informatics tools, and an expression experiment was conducted to verify their functions in vivo. Comparative genomic analysis revealed that 126 RGAs were included on chromosome 7A^uL, and 30 of the RGAs as well as Pm60 were found in the PmU region. Transcriptome database analysis of T. urartu revealed 14 PmU-RGAs with expression data, and three PmU-NBSs exhibited significant changes in expression after inoculation with Blumeria graminis f. sp. tritici (Bgt); TRIUR3_14879 was up-regulated, while TRIUR3_00450 and TRIUR3_06270 were down-regulated. Cluster analysis showed that these three PmU-NBSs were clustered far from the cloned wheat resistance genes. Then, qRT-PCR was performed to investigate the expression of 14 PmU-RGAs and Pm60 after inoculation with Bgt race E09; the results showed that Pm60 was specifically expressed in UR206 which carrying PmU, but not in susceptible UR203; while TRIUR3_14879 was significantly up-regulated and TRIUR3_00450 was downregulated in UR206 after inoculation. These results indicated that PmU is Pm60, and TRIUR3_14879 and TRIUR3_00450 may also be involved in the defense against Bgt.

Key words: cluster analysis , expression analysis , nucleotide binding site (NBS) , powdery mildew , protein kinase (PK)

. [J]. Journal of Integrative Agriculture, 2018, 17(12): 2601-2611.

ZHANG Lei, ZHENG Xing-wei, QIAO Lin-yi, QIAO Ling, ZHAO Jia-jia, WANG Jian-ming, ZHENG Jun. Analysis of three types of resistance gene analogs in PmU region from Triticum urartu[J]. Journal of Integrative Agriculture, 2018, 17(12): 2601-2611.

参考文献

Alvarez J B, Gutierrez M V, Guzman C, Martin L M. 2013. Molecular characterisation of the amino- and carboxyl-domains in different Glu-A1x alleles of Triticum urartu Thum. ex Gandil. Theoretical and Applied Genetics, 126, 1703–1711.
Arya P, Kumar G, Acharya V, Singh A K. 2014. Genome-wide identification and expression analysis of NBS-encoding genes in Malus×domestica and expansion of NBS genes family in Rosaceae. PLoS ONE, 9, e107987.
Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl J L. 2011. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proceedings of the National Academy of Sciences of the United States of America, 108, 16463–16468.
Cao A Z, Xing L P, Wang X Y, Yang X M, Wang W, Sun Y L, Qian C, Ni J L, Chen Y P, Liu D J, Wang X E, Chen P D. 2011. Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proceedings of the National Academy of Sciences of the United States of America, 108, 7727–7732.
Cloutier S, McCallum B D, Loutre C, Banks T W, Wicker T, Feuillet C, Keller B, Jordan M C. 2007. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Molecular Biology, 65, 93–106.
Collinge D B. 2009. Cell wall appositions: The first line of defence. Journal of Experimental Botany, 60, 351–352.
Ding J, Araki H, Wang Q, Zhang P, Yang S, Chen J Q, Tian D. 2007. Highly asymmetric rice genomes. BMC Genomics, 8, 154.
Douchkov D, Lück S, Johrde A, Nowara D, Himmelbach A, Rajaraman J, Stein N, Sharma R, Kilian B, Schweizer P. 2014. Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi. Genome Biology, 15, 518.
Dvorak J, Terlizzi P, Zhang H B, Resta P. 1993. The evolution of polyploid wheats: Identification of the A genome donor species. Genome, 36, 21–31.
Elmore J M, Lin Z J, Coaker G. 2011. Plant NB-LRR signaling: Upstreams and downstreams. Current Opinion in Plant Biology, 14, 365–371.
Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X M, Sela H, Fahima T, Dubcovsky J. 2009. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science, 323, 1357–1360.
Hammond-Kosack K E, Jones J G.1997. Plant disease resistance genes. Annual Review of Plant Biology, 48, 575–607.
Huang L, Brooks S A, Li W, Fellers J P, Trick H N, Gill B S. 2003. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics, 164, 655–664.
Jones J D, Dangl J L. 2006. The plant immune system. Nature, 444, 323–329.
Krattinger S G, Lagudah E S, Spielmeyer W, Singh R P, Huerta-Espino J, McFadden H, Bossolini E, Selter L L, Keller B. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323, 1360–1363.
Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Lee I, Seo Y S, Coltrane D, Hwang S, Oh T, Marcotte E M, Ronald P C. 2011. Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proceedings of the National Academy of Sciences of the United States of America, 108, 18548–18553.
Letunic I, Doerks T, Bork P. 2015. SMART: Recent updates, new developments and status in 2015. Nucleic Acids Research, 43, 257–260.
Li A L, Wang M L, Zhou R H, Kong X Y, Huo N X, Wang W S, Jia J Z. 2005. Comparative analysis of early H2O2 accumulation in compatible and incompatible wheat-powdery mildew interactions. Plant Pathology, 54, 308–316.
Ling H Q, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, et al. 2013. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature, 496, 87–90.
Liu W, Frick M, Huel R, Nykiforuk C L, Wang X, Gaudet D A, Eudes F, Conner R L, Kuzyk A, Chen Q, Kang Z, Laroche A. 2014. The stripe rust resistance gene Yr10 encodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Molecular Plant, 7, 1740–1755.
Ma H, Singh R P, Mujeeb-Kazi A. 1997. Resistance to stripe rust in durum wheats, A-genome diploids, and their amphiploids. Euphytica, 94, 279–286.
Mukhtar M S, Carvunis A R, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura M T, Pevzner S J, Donovan S E, Ghamsari L, Santhanam B, Romero V, Poulin M M, Gebreab F, Gutierrez B J, Tam S, Monachello D, et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science, 333, 596–601.
Mwale V M, Chilembwe E C, Uluko H C. 2014. Wheat powdery mildew (Blumeria graminis f. sp. tritici): Damage effects and genetic resistance developed in wheat (Triticum aestivum). International Research Journal of Plant Science, 5, 1–16.
Paillard S, Goldringer I, Enjalbert J, Trottet M, David J, de Vallavieille-Pope C, Brabant P. 2000. Evolution of resistance against powdery mildew in winter wheat populations conducted under dynamic management. I - Is specific seedling resistance selected? Theoretical and Applied Genetics, 101, 449–456.
Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M C, Kong X Y, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E. 2013. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science, 341, 786–788.
Pollier J, Rombauts S, Goossens A. 2013. Analysis of RNA-Seq data with TopHat and Cufflinks for genome-wide expression analysis of jasmonate-treated plants and plant cultures. Methods in Molecular Biology, 1011, 305–315.
Qiu Y C, Zhou R H, Kong X Y, Zhang S S, Jia J Z. 2005. Microsatellite mapping of a Triticum urartu Tum. derived powdery mildew resistance gene transferred to common wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 111, 1524–1531.
Rouse M N, Jin Y. 2011. Stem rust resistance in A-genome diploid relatives of wheat. Plant Disease, 95, 941–944.
Saintenac C, Zhang W, Salcedo A, Rouse M N, Trick H N, Akhunov E, Dubcovsky J. 2013. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science, 341, 783–786.
Santra M, Matthews S B, Thompson H J. 2013. Development of a core collection of Triticum and Aegilops species for improvement of wheat for activity against chronic diseases. Agriculture & Food Security, 2, 1–13.
Sarris P F, Duxbury Z, Huh S U, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet S B, Wirthmueller L, Menke F L, Sohn K H, Jones J D. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell, 161, 1089–1100.
Sela H, Spiridon L N, Petrescu A J, Akerman M, Mandel-Gutfreund Y, Nevo E, Loutre C, Keller B, Schulman A H, Fahima T. 2012. Ancient diversity of splicing motifs and protein surfaces in the wild emmer wheat (Triticum dicoccoides) LR10 coiled coil (CC) and leucine-rich repeat (LRR) domains. Molecular Plant Pathology, 13, 276–287.
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.
Steuernagel B, Periyannan S K, Hernández-Pinzón I, Witek K, Rouse M N, Yu G, Hatta A, Ayliffe M, Bariana H, Jones J D, Lagudah E S, Wulff B B. 2016. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nature Biotechnology, 34, 652–665.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
The Rice Chromosomes 11 and 12 Sequencing Consortia. 2005. The sequence of rice chromosomes 11 and 12 rich in disease resistance genes and recent gene duplications. BMC Biology, 3, 1–18.
Tommasini L, Yahiaoui N, Srichumpa P, Keller B. 2006. Development of functional markers specific for seven Pm3 resistance alleles and their validation in the bread wheat gene pool. Theoretical and Applied Genetics, 114, 165–175.
Trapnell C, Pachter L, Salzberg S L. 2009. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105–1111.
Wäspi U, Schweizer P, Dudler R. 2001. Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew. The Plant Cell, 13, 153–161.
Wheeler T J, Eddy S R. 2013. nhmmer: DNA homology search with profile HMMs. Bioinformatics, 29, 2487–2489.
Wolter M, Hollricher K, Salamini F, Schulze-Lefert P. 1993. The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defense mimic phenotype. Molecular Genetics and Genomics, 239, 122–128.
Yahiaoui N, Srichumpa P, Dudler R, Keller B. 2004. Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. The Plant Journal, 37, 528–538.
Yu J, Tehrim S, Zhang F, Tong C, Huang J, Cheng X, Dong C, Zhou Y, Qin R, Hua W, Liu S. 2014. Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genomics, 15, 3.
Zhang J, Zheng H, Li Y, Li H, Liu X, Qin H, Dong L, Wang D. 2016. Coexpression network analysis of the genes regulated by two types of resistance responses to powdery mildew in wheat. Scientific Reports, 6, 23805.
Zhang R, Sun B, Chen J, Cao A Z, Xing L P, Feng Y, Lan C, Chen P D. 2016. Pm55, a developmental-stage and tissue-specific powdery mildew resistance gene introgressed from Dasypyrum villosum into common wheat. Theoretical and Applied Genetics, 129, 1975–1984.
Zipfel C. 2009. Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology, 12, 414–420.
Zou S H, Wang H, Li Y W, Kong Z S, Tang D Z. 2017. The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytologist, 218, 298–309.