Integrative Molecular Approaches to Plant Disease: A Review

Prashanth Kumar A. *

JVR Horticultural Research Station, Malyal, SKLTSHU, India.

Nikhil B. S. K.

JVR Horticultural Research Station, Malyal, SKLTSHU, India.

*Author to whom correspondence should be addressed.


Abstract

Modern molecular and bioinformatics technologies have made understanding host-pathogen interactions easier. Plants have many ways to protect themselves from microbial diseases, such as physical barriers, PAMP detection, and R genes that recognize pathogen-effector proteins and turn on effector-triggered immunity. Plant pathogen genome databases provide genomic and phenotypic data on plant pathogen species and information on plant-pathogen interactions. Map-based or positional gene cloning is improving our understanding of plant-pathogen interactions, with R genes being used to develop resistance to pathogens. Plant genomes typically contain several hundred nucleotide-binding site-leucine-rich repeats (NLRs), with their number, arrangement, and domain combinations varying by species. Bacterial blight (BB) severely impacts rice production, and about 37 of 44 resistance genes have been mapped and 15 cloned. Many disease-resistant wheat cultivars have been developed using powdery mildew leaf rust (Lr) resistance genes from wild relatives of T. aestivum. Over 140 genes are linked to powdery mildew resistance in T. aestivum and MutChromSeq have found new target genes. Cloning Arabidopsis resistance genes is essential for developing resistant cultivars and understanding R gene evolution. Some R genes encode proteins with nucleotide-binding site (NBS) motifs, and an LRR protects against Erysiphe cruciferarum powdery mildew. CRISPR/Cas9 gene editing is a major tool in plant genome editing, efficiently introducing target site mutations and improving plant immunity. High-throughput sequencing can identify and clone candidate resistance genes in different plant species, and gene editing technologies like CRISPR/Cas have illuminated site-specific mutagenesis and durable resistance.

Keywords: Defense, database, pathogen, resistance genes and clone


How to Cite

Prashanth Kumar A., & Nikhil B. S. K. (2023). Integrative Molecular Approaches to Plant Disease: A Review. International Journal of Environment and Climate Change, 13(10), 2803–2812. https://doi.org/10.9734/ijecc/2023/v13i102945

Downloads

Download data is not yet available.

References

Ali Q, Zheng H, Rao MJ, Ali M, Hussain A, Saleem MH, et al. Advances, limitations, and prospects of biosensing technology for detecting phytopathogenic bacteria. Chemosphere. 2022;296: 133773.

Mu H, Wang B, Yuan F. Bioinformatics in Plant Breeding and Research on Disease Resistance. Plants. 2022;11:3118.

Boutrot F, Zipfel C. Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 2017; 55:257–286.

Srivastava D, Shamim M, Kumar M, Mishra A, Pandey P, Kumar D, et al. Current status of conventional and molecular interventions for blast resistance in rice. Rice Sci. 2017;24:299–321.

Wei C, Kuang H, Li F, Chen J. The I2 resistance gene homologues in Solanum have complex evolutionary patterns and are targeted by miRNAs. BMC Genom. 2014;15:743.

Hatsugai N, Hillmer R, Yamaoka S, Hara-Nishimura I, Katagiri F. The µ Subunit of Arabidopsis Adaptor Protein-2 Is Involved in Effector-Triggered Immunity Mediated by Membrane-Localized Resistance Proteins. Mol. Plant Microbe Interact. 2016;29:345–351.

Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995;270: 1804–1806.

Johal GS, Briggs SP. Reductase activity encoded by the HM1 disease resistance gene in maize. Science. 1992;258:985–987.

Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 1999;19:55–64.

Qu S, Liu G, Zhou B, Bellizzi M, Zeng L, Dai L, et al. The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics. 2006;172:1901–1914.

Yadav MK, Aravindan S, Ngangkham U, Raghu S, Prabhukarthikeyan SR, Keerthana U, et al. Blast resistance in Indian rice landraces: Genetic dissection by gene specific markers. PLoS ONE. 2019;14:e0211061.

Liu X, Lin F, Wang L, Pan Q. The in-silico map-based cloning of Pi36, a rice coiled-coil nucleotide-binding site leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics. 2007;176:2541–2549.

Hurni S, Brunner S, Buchmann G, Herren G, Jordan T, Krukowski P, et al. Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J. 2013;76:957–969.

Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, Adamski N, et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 2016;17:221.

Steuernage B, Vrána J, Karafiátová M, Wulff BBH, Doležel J. Rapid Gene Isolation Using Mut Chrom Seq. Methods Mol. Biol. 2017;1659:231–243.

Xing L, Hu P, Liu J, Witek K, Zhou S, Xu J, Zhou W, et al. Pm21 from Haynaldia villosa Encodes a CC-NBS-LRR Protein Conferring Powdery Mildew Resistance in Wheat. Mol. Plant. 2018;11:874–878.

Xie J, Guo G, Wang Y, Hu T, Wang L, Li J, et al. A rare single nucleotide variant in Pm5e confers powdery mildew resistance in common wheat. New Phytol. 2020; 228:1011–1026.

Yang Y, Zhou Y, Sun J, Liang W, Chen X, et al. Research Progress on Cloning and Function of Xa Genes Against Rice Bacterial Blight. Front Plant Sci. 2022; 13:847199.

Karmakar S, Das P, Panda D, Xie K, Baig MJ, Molla KA. A detailed landscape of CRISPR-Cas-mediated plant disease and pest management. Plant Sci. 2022;323: 111376.

Pedro H, Maheswari U, Urban M, Irvine AG, Cuzick A, McDowall MD, et al. PhytoPath: An integrative resource for plant pathogen genomics. Nucleic Acids Res. 2016;44:D688–D693.

Takeya M, Yamasaki F, Uzuhashi S, Aoki T, Sawada H, Nagai T, et al. NIASGBdb: NIAS Genebank databases for genetic resources and plant disease information. Nucleic Acids Res. 2011;39:D1108–D1113.

Urban M, Cuzick A, Seager J, Wood V, Rutherford K, Venkatesh SY, et al. PHI-base in 2022: A multi-species phenotype database for Pathogen-Host Interactions. Nucleic Acids Res. 2022;50:D837–D847.

Dong AY, Wang Z, Huang JJ, Song BA, Hao GF. Bioinformatic tools support decision-making in plant disease management. Trends Plant Sci. 2021;26:953–967.

Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG. The L6 Gene for Flax Rust Resistance Is Related to the Arabidopsis Bacterial Resistance Gene RPS2 and the Tobacco Viral Resistance Gene N. Plant Cell. 1995;7:1195–1206.

Kourelis J, van der Hoorn RAL. Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function. Plant Cell. 2018;30:285–299.

Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell. 2005;15:809–834.

Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J. Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genom. 2013;14:109.

Lin X, Zhang Y, Kuang H, Chen J. Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae. BMC Genom. 2013;14: 335.

Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, et al. The genome of the domesticated apple (Malus domestica Borkh.). Nat. Genet. 2010;42: 833–839.

Baggs E, Dagdas G, Krasileva KV. NLR diversity, helpers and integrated domains: Making sense of the NLR identity. Curr. Opin. Plant Biol. 2017;38:59–67.

Chen L, Yin F, Zhang D, Xiao S, Zhong Q, Wang B, et al. Unveiling a Novel Source of Resistance to Bacterial Blight in Medicinal Wild Rice, Oryza officinalis. Life. 2022; 12:827.

Liu G, Lu G, Zeng L, Wang GL. Two broad-spectrum blast resistance genes, Pi9(t) and Pi2(t), are physically linked on rice chromosome 6. Mol. Genet Genom. 2002;267:472–480. [CrossRef]

Shang J, Tao Y, Chen X, Zou Y, Lei C, Wang J, Li X, et al. Identification of a new rice blast resistance gene, Pid3, by genome wide comparison of paired nucleotide-binding site--leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics. 2009;182:1303–1311.

Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, et al. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. 2011;66:467–479.

Das A, Soubam D, Singh PK, Thakur S, Singh NK, Sharma TR. A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct. Integr. Genom. 2012;12: 215–228.

Chen J, Shi Y, Liu W, Chai R, Fu Y, Zhuang J, Wu J. A Pid3 allele from rice cultivar Gumei2 confers resistance to Magnaporthe oryzae. J. Genet Genom. 2011;38:209–216.

Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B. Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc. Natl. Acad. Sci. USA. 2003;100:15253–15258.

Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics. 2003;164:655–664.

Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, et al. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol. Biol. 2007;65:93–106.

Brunner S, Hurni S, Streckeisen P, Mayr G, Albrecht M, Yahiaoui N, Keller B. Intragenic allele pyramiding combines different specificities of wheat Pm3 resistance alleles. Plant J. 2010;64:433–445.

Yahiaoui N, Srichumpa P, Dudler R, Keller B. Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J. 2004;37:528–538.

Srichumpa P, Brunner S, Keller B, Yahiaoui N. Allelic series of four powdery mildew resistance genes at the Pm3 locus in hexaploid bread wheat. Plant Physiol. 2004;139:885–895.

Singh SP, Hurni S, Ruinelli M, Brunner S, Sanchez-Martin J, Krukowski P, et al. Evolutionary divergence of the rye Pm17 and Pm8 resistance genes reveals ancient diversity. Plant Mol. Biol. 2018;98:249–260.

Lu P, Guo L, Wang Z, Li B, Li J, Li Y, et al. A rare gain of function mutation in a wheat tandem kinase confers resistance to powdery mildew. Nat. Commun. 2020;11: 680.

Li M, Dong L, Li B, Wang Z, Xie J, Qiu D, et al. A CNL protein in wild emmer wheat confers powdery mildew resistance. New Phytol. 2020;228:1027–1037.

Zou S, Shi W, Ji J, Wang H, Tang Y, Yu D, Tang D. Diversity and similarity of wheat powdery mildew resistance among three allelic functional genes at the Pm60 locus. Plant J. 2022;110:1781–1790.

Zou S, Wang H, Li Y, Kong Z, Tang D. The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. New Phytol. 2018;218:298–309.

Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 2015;47:1494–1498.

Krattinger SG, Kang J, Bräunlich S, Boni R, Chauhan H, Selter LL, et al. Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytol. 2019; 223:853–866.

Deng C, Leonard A, Cahill J, Lv M, Li Y, Thatcher S, et al. The RppC-AvrRppC NLR-effector interaction mediates the resistance to southern corn rust in maize. Mol. Plant. 2022;15:904–912.

Li N, Lin B, Wang H, Li X, Yang F, Ding X, et al. Natural variation in ZmFBL41 confers banded leaf and sheath blight resistance in maize. Nat. Genet. 2019;51:1540–1548.

Wang H, Hou J, Ye P, Hu L, Huang J, Dai Z, et al. A teosinte-derived allele of a MYB transcription repressor confers multiple disease resistance in maize. Mol. Plant. 2021;14:1846–1863.

Liu Q, Liu H, Gong Y, Tao Y, Jiang L, Zuo W, et al. An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize. Mol. Plant. 2017;10:483–497.

Leng P, Ji Q, Asp T, Frei UK, Ingvardsen CR, Xing Y, et al. Auxin Binding Protein 1 Reinforces Resistance to Sugarcane Mosaic Virus in Maize. Mol. Plant. 2017; 10:1357–1360.

Gómez-Gómez L, Boller T. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell. 2000;5:1003–1011.

Kim MH, Kim Y, Kim JW, Lee HS, Lee WS, Kim SK, et al. Identification of Arabidopsis BAK1-associating receptor-like kinase 1 (BARK1) and characterization of its gene expression and brassinosteroid-regulated root phenotypes. Plant Cell Physiol. 2013;54:1620–1634.

Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, et al. RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science. 1994;265:1856–1860.

Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, et al. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995;269:843–846.

McDowell JM, Dhandaydham M, Long TA, Aarts MG, Goff S, Holub EB, Dangl JL. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell. 1998; 10:1861–1874.

Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000;21:177–188.

Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA. 1998;95:10306–10311.

Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science. 1997;278:1963–1965.

Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, et al. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 2002; 32:655–667.

Bashir S, Rehman N, Fakhar Zaman F, Naeem MK, Jamal A, Tellier A, et al. Genome-wide characterization of the NLR gene family in tomato (Solanum lycopersicum) and their relatedness to disease resistance. Front. Genet. 2022; 13:931580.

Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. USA. 2002;99:2404–2409.

Steuernagel B, Jupe F, Witek K, Jones JD Wulff BB. NLR-parser: Rapid annotation of plant NLR complements. Bioinformatics. 2015;31:1665–1667.

Huang Z, Qiao F, Yang B, Liu J, Liu Y, Wulff BBH, Hu P, et al. Genome-wide identification of the NLR gene family in Haynaldia villosa by SMRT-RenSeq. BMC Genom. 2022;23:118.

Toda N, Rustenholz C, Baud A, Le Paslier MC, Amselem J, Merdinoglu D, Faivre-Rampant P. NL Genome Sweeper: A Tool for Genome-Wide NBS-LRR Resistance Gene Identification. Genes. 2020;11:333.

Jupe F, Witek K, Verweij W, Sliwka J, Pritchard L, Etherington GJ, et al. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 2013;76:530–544.

Kourelis J, Sakai T, Adachi H, Kamoun S. Ref Plant NLR: A comprehensive collection of experimentally validated plant NLRs. PLoS Biol. 2021;19:e3001124.

Armario Najera V, Twyman RM, Christou P, Zhu C. Applications of multiplex genome editing in higher plants. Curr Opin Biotechnol. 2019;59:93–102.

Li C, Chu W, Gill RA, Sang S, Shi Y, Hu X, et al. Computational tools and resources for CRISPR/Cas genome editing. Genom. Proteom. Bioinform. 2022;S1672-0229(22) 00027-4.

Fister AS, Landherr L, Maximova SN, Guiltinan MJ. Transient expression of CRISPR/Cas9 machinery targeting TcNPR3 enhances defense response in Theobroma cacao. Front. Plant Sci. 2018; 9:268.

Sun Q, Lin L, Liu D, Wu D, Fang Y, Wu J, Wang Y. CRISPR/Cas9-Mediated multiplex genome editing of the BnWRKY11 and BnWRKY70 genes in Brassica napus L. Int. J. Mol. Sci. 2018; 19:2716.

Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 2014; 32:947–951.

Santillán Martínez MI, Bracuto V, Koseoglou E, Appiano M, Jacobsen E, et al. CRISPR/Cas9- targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew. BMC Plant Biol. 2020;20:284.

Jarosch B, Kogel KH, Schaffrath U. The ambivalence of the barley Mlo locus: Mutations conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact. 1999;12:508– 514.

Wan DY, Guo Y, Cheng Y, Hu Y, Xiao S, Wang Y, Wen YQ. CRISPR/Cas9-mediated mutagenesis of VvMLO3 results in enhanced resistance to powdery mildew in grapevine (Vitis vinifera). Hortic. Res. 2020;7:116.

Zhang Y, Bai Y, Wu G, Zou S, Chen Y, Gao C, Tang D. Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant J. 2017;91:714–724.

Liu D, Chen X,Liu J, Ye J, Guo Z. The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J. Exp. Bot. 2012;63:3899–3912.

Lu W, Deng F, Jia J, Chen X, Li J, Wen Q, Li T, et al. The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity. Mol. Plant Pathol. 2020;21:1179–1193.

Langen G, von Einem S, Koch A, Imani J, Pai SB, Manohar M, et al. The compromised recognition of turnip crinkle virus1 subfamily of microrchidia ATPases regulates disease resistance in barley to biotrophic and necrotrophic pathogens. Plant Physiol. 2014;164:866–878.

Kumar N, Galli M, Ordon J, Stuttmann J, Kogel KH, Imani J. Further analysis of barley MORC1 using a highly efficient RNA-guided Cas9 gene-editing system. Plant Biotechnol. J. 2018;16:1892–1903.

Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS ONE. 2011;6:e29595.

Rodríguez-Hernández AM, Gosalvez B, Sempere RN, Burgos L, Aranda MA, Truniger V. Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Mol. Plant Pathol. 2012;13:755–763.

Ma S, Lapin D, Liu L, Sun Y, Song W, Zhang X, et al. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science. 2020;370:eabe3069.

Martin R, Qi T, Zhang H, Liu F, King M, Toth C, Nogales E, Staskawicz BJ. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science. 2020; 370:eabd9993.

Li S, Shen L, Hu P, Liu Q, Zhu X, Qian Q, Wang K, Wang Y. Developing disease-resistant thermosensitive male sterile rice by multiplex gene editing. J. Integr. Plant Biol. 2019;61:1201–1205.

Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X. Engineering canker-resistant plants through CRISPR/Cas9- targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol. J. 2017;15:1509–1519.

Ahn HK, Lin X, Olave-Achury AC, Derevnina L, Contreras MP, Kourelis J, et al. Effector- dependent activation and oligomerization of plant NRC class helper NLRs by sensor NLR immune receptors Rpi-amr3 and Rpi-amr1. EMBO J. 2023, 42, e111484.

Joshi A, Yang SY, Lee JH. Integrated Molecular and Bioinformatics Approaches for Disease-Related Genes in Plants. Plants. 2023;12:245.