Integrated transcriptomics and metabolomics reveal induction of hierarchies of resistance genes in potato against late blight
Kalenahalli N. Yogendra A and Ajjamada C. Kushalappa A B
+ Author Affiliations
- Author Affiliations
A Department of Plant Science, McGill University, Ste. Anne de Bellevue, Québec, Canada.
B Corresponding author. Email: ajjamada.kushalappa@mcgill.ca
Functional Plant Biology 43(8) 766-782 https://doi.org/10.1071/FP16028
Submitted: 23 January 2016 Accepted: 15 April 2016 Published: 18 May 2016
Abstract
Late blight caused by Phytophthora infestans is a devastating disease affecting potato production worldwide. The quantitative resistance is durable, but the underlying molecular and biochemical mechanisms are poorly understood, limiting its application in breeding. Integrated transcriptomics and metabolomics approach was used for the first time to study the hierarchies of molecular events occurring, following inoculation of resistant and susceptible potato genotypes with P. infestans. RNA sequencing revealed a total of 4216 genes that were differentially expressed in the resistant than in the susceptible genotype. Genes that were highly expressed and associated with their biosynthetic metabolites that were highly accumulated, through metabolic pathway regulation, were selected. Quantitative real-time PCR was performed to confirm the RNA-seq expression levels. The induced leucine-rich repeat receptor-like kinases (LRR-RLKs) are considered to be involved in pathogen recognition. These receptor genes are considered to trigger downstream oxidative burst, phytohormone signalling-related genes, and transcription factors that regulated the resistance genes to produce resistance related metabolites to suppress the pathogen infection. It was noted that several resistance genes in metabolic pathways related to phenylpropanoids, flavonoids, alkaloids and terpenoid biosynthesis were strongly induced in the resistant genotypes. The pathway specific gene induction provided key insights into the metabolic reprogramming of induced defence responses in resistant genotypes.
Additional keywords: biotic stress, metabolomics, Phytophthora infestans, quantitative resistance, RNA sequencing, transcriptomics.
References
Agudelo-Romero P, Erban A, Rego C, Carbonell-Bejerano P, Nascimento T, Sousa L, Martínez-Zapater JM, Kopka J, Fortes AM (2015) Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea. Journal of Experimental Botany| Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 25675955PubMed |
Ali A, Alexandersson E, Sandin M, Resjö S, Lenman M, Hedley P, Levander F, Andreasson E (2014) Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions. BMC Genomics 15, 497
| Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions.Crossref | GoogleScholarGoogle Scholar | 24947944PubMed |
Alves MS, Dadalto SP, Gonçalves AB, De Souza GB, Barros VA, Fietto LG (2013) Plant bZIP transcription factors responsive to pathogens: a review. International Journal of Molecular Sciences 14, 7815–7828.
| Plant bZIP transcription factors responsive to pathogens: a review.Crossref | GoogleScholarGoogle Scholar | 23574941PubMed |
Alves MS, Dadalto SP, Gonçalves AB, de Souza GB, Barros VA, Fietto LG (2014) Transcription factor functional protein–protein interactions in plant defense responses. Proteomes 2, 85–106.
| Transcription factor functional protein–protein interactions in plant defense responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtlWls7o%3D&md5=d9c0d269e7d9bb14d41d3f2fdacd35d6CAS |
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiology and Molecular Biology of Plants 19, 307–321.
| MYB transcription factor genes as regulators for plant responses: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFGrsb7O&md5=4b9d10bc3396e491a9e3f520c592a3edCAS | 24431500PubMed |
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biology 11, R106
| Differential expression analysis for sequence count data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVahs7bI&md5=f46d8f0e62cab0f432a38d8e2f6b9eddCAS | 20979621PubMed |
Andrivon D, Corbière R, Lucas J-M, Pasco C, Gravoueille J-M, Pellé R, Dantec J-P, Ellissèche D (2003) Resistance to late blight and soft rot in six potato progenies and glycoalkaloid contents in the tubers. American Journal of Potato Research 80, 125–134.
| Resistance to late blight and soft rot in six potato progenies and glycoalkaloid contents in the tubers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1Kmsbc%3D&md5=826338836eea7fd4bc4be262dfb176f0CAS |
Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. The Plant Cell 20, 1390–1406.
| MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlyrtL8%3D&md5=4d941448de131608de63029626b20cb7CAS | 18515503PubMed |
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT (2000) Gene Ontology: tool for the unification of biology. Nature Genetics 25, 25–29.
| Gene Ontology: tool for the unification of biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFSlsbc%3D&md5=79002c74e5a87d6ec3295f7d9ee54a2bCAS | 10802651PubMed |
Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H (2011) Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breeding Science 61, 121–129.
| Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2js7jL&md5=17ef2092e23198f7f3bd9ee11dc8c7b1CAS |
Ballvora A, Ercolano MR, Weiß J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. The Plant Journal 30, 361–371.
| The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xks1Oht78%3D&md5=cf4fc706edf47d96f4630dcffc9a717cCAS | 12000683PubMed |
Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylidès C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. The Plant Journal 13, 519–527.
| Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitFyrs7w%3D&md5=10e1e6ca64d9179a92588c27bfe2aa64CAS | 9680997PubMed |
Bethke PC, Nassar AM, Kubow S, Leclerc YN, Li X-Q, Haroon M, Molen T, Bamberg J, Martin M, Donnelly DJ (2014) History and origin of Russet Burbank (Netted Gem) a sport of Burbank. American Journal of Potato Research 91, 594–609.
| History and origin of Russet Burbank (Netted Gem) a sport of Burbank.Crossref | GoogleScholarGoogle Scholar |
Bollina V, Kumaraswamy GK, Kushalappa AC, Choo TM, Dion Y, Rioux S, Faubert D, Hamzehzarghani H (2010) Mass spectrometry‐based metabolomics application to identify quantitative resistance‐related metabolites in barley against Fusarium head blight. Molecular Plant Pathology 11, 769–782.
Brueggeman R, Druka A, Nirmala J, Cavileer T, Drader T, Rostoks N, Mirlohi A, Bennypaul H, Gill U, Kudrna D (2008) The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. Proceedings of the National Academy of Sciences of the United States of America 105, 14970–14975.
| The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aqurzN&md5=da3b5d2b1b72685a7a91e0c353a2ba94CAS | 18812501PubMed |
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences of the United States of America 107, 9452–9457.
| A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslamsrk%3D&md5=abea7d3ca5cf2da2769ca31e69922fa2CAS | 20439716PubMed |
Burra DD, Berkowitz O, Hedley PE, Morris J, Resjö S, Levander F, Liljeroth E, Andreasson E, Alexandersson E (2014) Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans. BMC Plant Biology 14, 254
| Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 25270759PubMed |
Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu 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.
| Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVSktrg%3D&md5=3b764d7b3f7bbfa1a3de6adafda366f3CAS | 21508323PubMed |
Chen Y, Halterman DA (2011) Phenotypic characterization of potato late blight resistance mediated by the broad-spectrum resistance gene RB. Phytopathology 101, 263–270.
| Phenotypic characterization of potato late blight resistance mediated by the broad-spectrum resistance gene RB.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitVeqsrk%3D&md5=137801eed295e25f412589ba89ec919cCAS | 20923366PubMed |
Coulombe P, Meloche S (2007) Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research 1773, 1376–1387.
| Atypical mitogen-activated protein kinases: structure, regulation and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFyktro%3D&md5=4a423b182d17ba188055a04177b0b36eCAS |
De Vos RC, Moco S, Lommen A, Keurentjes JJ, Bino RJ, Hall RD (2007) Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry. Nature Protocols 2, 778–791.
| Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGntbfE&md5=fc3fba634a2a14b36eb79375ee67b58eCAS | 17446877PubMed |
Docimo T, Mattana M, Fasano R, Consonni R, De Tommasi N, Coraggio I, Leone A (2013) Ectopic expression of the Osmyb4 rice gene enhances synthesis of hydroxycinnamic acid derivatives in tobacco and clary sage. Biologia Plantarum 57, 179–183.
| Ectopic expression of the Osmyb4 rice gene enhances synthesis of hydroxycinnamic acid derivatives in tobacco and clary sage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnt12lurg%3D&md5=54e4fe184d6caf6dc83bfb3038bf7c7eCAS |
Elmore JM, Lin Z-JD, Coaker G (2011) Plant NB-LRR signaling: upstreams and downstreams. Current Opinion in Plant Biology 14, 365–371.
| Plant NB-LRR signaling: upstreams and downstreams.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVWmt77P&md5=508313be38bcd27156f1551054cf9e43CAS | 21459033PubMed |
Etalo DW, Stulemeijer IJ, van Esse HP, de Vos RC, Bouwmeester HJ, Joosten MH (2013) System-wide hypersensitive response-associated transcriptome and metabolome reprogramming in tomato. Plant Physiology 162, 1599–1617.
| System-wide hypersensitive response-associated transcriptome and metabolome reprogramming in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCmtLbK&md5=2721fccdca68ebe70212a06926b1b7feCAS | 23719893PubMed |
Eudes A, Liang Y, Mitra P, Loque D (2014) Lignin bioengineering. Current Opinion in Biotechnology 26, 189–198.
| Lignin bioengineering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1Cktb0%3D&md5=9927954b326aa715c9420950f76e547cCAS | 24607805PubMed |
Farré G, Twyman RM, Christou P, Capell T, Zhu C (2015) Knowledge-driven approaches for engineering complex metabolic pathways in plants. Current Opinion in Biotechnology 32, 54–60.
| Knowledge-driven approaches for engineering complex metabolic pathways in plants.Crossref | GoogleScholarGoogle Scholar | 25448233PubMed |
Feussner I, Polle A (2015) What the transcriptome does not tell – proteomics and metabolomics are closer to the plants’ patho-phenotype. Current Opinion in Plant Biology 26, 26–31.
| What the transcriptome does not tell – proteomics and metabolomics are closer to the plants’ patho-phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpt1Krurc%3D&md5=1d970cb64c6ee2eb35e43a9077d09e9eCAS | 26051215PubMed |
Foster SJ, Park T-H, Pel M, Brigneti G, Sliwka J, Jagger L, van der Vossen E, Jones JD (2009) Rpi-vnt1. 1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Molecular Plant-Microbe Interactions 22, 589–600.
| Rpi-vnt1. 1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Wns7g%3D&md5=5873569340abbc9e327a5ed5133482a7CAS | 19348576PubMed |
Fountain JC, Raruang Y, Luo M, Brown RL, Guo B, Chen Z-Y (2015) Potential roles of WRKY transcription factors in regulating host defense responses during Aspergillus flavus infection of immature maize kernels. Physiological and Molecular Plant Pathology 89, 31–40.
| Potential roles of WRKY transcription factors in regulating host defense responses during Aspergillus flavus infection of immature maize kernels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVyktLbI&md5=790e541dc242510b757068568a45b7bcCAS |
Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323, 1357–1360.
| A kinase-START gene confers temperature-dependent resistance to wheat stripe rust.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemtb0%3D&md5=653b03aea28b4af03b32e676e4814598CAS | 19228999PubMed |
Gallego‐Giraldo L, Jikumaru Y, Kamiya Y, Tang Y, Dixon RA (2011) Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytologist 190, 627–639.
| Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1enurc%3D&md5=ba631b59ec4bc0e93dfec807c9e9e4bbCAS | 21251001PubMed |
Gamboa-Meléndez H, Huerta AI, Judelson HS (2013) bZIP transcription factors in the oomycete Phytophthora infestans with novel DNA-binding domains are involved in defense against oxidative stress. Eukaryotic Cell 12, 1403–1412.
| bZIP transcription factors in the oomycete Phytophthora infestans with novel DNA-binding domains are involved in defense against oxidative stress.Crossref | GoogleScholarGoogle Scholar | 23975888PubMed |
Gao Q-M, Venugopal S, Navarre D, Kachroo A (2011) Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiology 155, 464–476.
| Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagt7Y%3D&md5=740a1a0d014aa97649d0e39c332d9d62CAS | 21030507PubMed |
Gao L, Tu ZJ, Millett BP, Bradeen JM (2013) Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber–Phytophthora infestans interactions. BMC Genomics 14, 340
| Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber–Phytophthora infestans interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVOrtL3O&md5=11d859f2c8f8102551405ddf5b41d915CAS | 23702331PubMed |
Gebhardt C (2013) Bridging the gap between genome analysis and precision breeding in potato. Trends in Genetics 29, 248–256.
| Bridging the gap between genome analysis and precision breeding in potato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVymu7vP&md5=0869d77f4ecc9abe9a80683a5460f100CAS | 23261028PubMed |
Giron D, Frago E, Glevarec G, Pieterse CM, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Functional Ecology 27, 599–609.
| Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence.Crossref | GoogleScholarGoogle Scholar |
Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signaling in Arabidopsis. The Plant Cell 13, 1155–1163.
| Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11340188PubMed |
Gunnaiah R, Kushalappa AC, Duggavathi R, Fox S, Somers DJ (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS One 7, e40695
| Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOnsL%2FL&md5=b53e8fc0b1cb63a150876816cd2aae5dCAS | 22866179PubMed |
Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology 7, 465–471.
| Regulation of disease resistance pathways by AP2/ERF transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVWhurg%3D&md5=9444553fb5b01d651dca96ddda15c564CAS | 15231271PubMed |
Haverkort A, Struik P, Visser R, Jacobsen E (2009) Applied biotechnology to combat late blight in potato caused by Phytophthora infestans. Potato Research 52, 249–264.
| Applied biotechnology to combat late blight in potato caused by Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar |
Huang S, Van Der Vossen EA, Kuang H, Vleeshouwers VG, Zhang N, Borm TJ, Van Eck HJ, Baker B, Jacobsen E, Visser RG (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. The Plant Journal 42, 251–261.
| Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvFSrtrs%3D&md5=a7badf1c559db26282d2cfd3c0c71986CAS | 15807786PubMed |
Ishiga Y, Uppalapati SR, Gill US, Huhman D, Tang Y, Mysore KS (2015) Transcriptomic and metabolomic analyses identify a role for chlorophyll catabolism and phytoalexin during Medicago non-host resistance against Asian soybean rust. Scientific Reports 5, 1–17.
| Transcriptomic and metabolomic analyses identify a role for chlorophyll catabolism and phytoalexin during Medicago non-host resistance against Asian soybean rust.Crossref | GoogleScholarGoogle Scholar |
Jo K-R, Kim C-J, Kim S-J, Kim T-Y, Bergervoet M, Jongsma MA, Visser RG, Jacobsen E, Vossen JH (2014) Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnology 14, 50
| Development of late blight resistant potatoes by cisgene stacking.Crossref | GoogleScholarGoogle Scholar | 24885731PubMed |
Jones JD, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=8c3478940ede75d28698c9946ce7d46eCAS | 17108957PubMed |
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Research 36, D480–D484.
| KEGG for linking genomes to life and the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSku7k%3D&md5=a31d79ab8e0da608b0d1ede23a0ebc3eCAS | 18077471PubMed |
Kang S, Yang F, Li L, Chen H, Chen S, Zhang J (2015) The Arabidopsis transcription factor BES1 is a direct substrate of MPK6 and regulates immunity. Plant physiology 167, 1076–1086.
| The Arabidopsis transcription factor BES1 is a direct substrate of MPK6 and regulates immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1aqtL8%3D&md5=aa9f2ad9722733305e37dd24f86a94c1CAS | 25609555PubMed |
Kohorn BD, Kohorn SL (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science 3, 1–5.
| The cell wall-associated kinases, WAKs, as pectin receptors.Crossref | GoogleScholarGoogle Scholar |
Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Current Opinion in Plant Biology 13, 181–185.
| Broad-spectrum and durability: understanding of quantitative disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFahs7w%3D&md5=81409525caebd92585b3c7c117a105dbCAS | 20097118PubMed |
Kumaraswamy G, Kushalappa A, Choo T, Dion Y, Rioux S (2012) Differential metabolic response of barley genotypes, varying in resistance, to trichothecene‐producing and‐nonproducing (tri5− ) isolates of Fusarium graminearum. Plant Pathology 61, 509–521.
| Differential metabolic response of barley genotypes, varying in resistance, to trichothecene‐producing and‐nonproducing (tri5− ) isolates of Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVeit7rF&md5=c77e514a90c5da436c8daebc085cb7caCAS |
Kushalappa AC, Gunnaiah R (2013) Metabolo-proteomics to discover plant biotic stress resistance genes. Trends in Plant Science 18, 522–531.
| Metabolo-proteomics to discover plant biotic stress resistance genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslKktb4%3D&md5=d9b3af620381fa6155d1fe0dca7ebf54CAS | 23790252PubMed |
Kushalappa AC, Yogendra KN, Karre S (2016) Plant innate immune response: qualitative and quantitative resistance. Critical Reviews in Plant Sciences 35, 38–55.
| Plant innate immune response: qualitative and quantitative resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xltlajurk%3D&md5=d01f2c30223cb582227646c26213af79CAS |
Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T, Seo M, Kanno Y, Häkkinen ST, Van Montagu MC (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proceedings of the National Academy of Sciences of the United States of America 108, 5891–5896.
| Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVCmtbY%3D&md5=3f6da99edfdb34fef1e1d59720a86366CAS | 21436041PubMed |
Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary cell wall architecture. Plant Physiology 156, 11–19.
| Role of the extensin superfamily in primary cell wall architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVWgtr4%3D&md5=37c1666031c4e2f99ce606af4b7d3bf8CAS | 21415277PubMed |
Li G, Huang S, Guo X, Li Y, Yang Y, Guo Z, Kuang H, Rietman H, Bergervoet M, Vleeshouwers VG (2011) Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. Molecular Plant-Microbe Interactions 24, 1132–1142.
| Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Wjt7rK&md5=a6c99fa256bde943301b1b7ad51f59caCAS | 21649512PubMed |
Li R, Tee C-S, Jiang Y-L, Jiang X-Y, Venkatesh PN, Sarojam R, Ye J (2015) A terpenoid phytoalexin plays a role in basal defense of Nicotiana benthamiana against Potato virus X. Scientific Reports 5, 1–6.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=3c52ba31a95ed35024a5c40b81df18e8CAS | 11846609PubMed |
Lokossou AA, Park T-h, van Arkel G, Arens M, Ruyter-Spira C, Morales J, Whisson SC, Birch PR, Visser RG, Jacobsen E (2009) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Molecular Plant-Microbe Interactions 22, 630–641.
| Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGktrY%3D&md5=cb85dd1b458c333667b90425cb45f27eCAS | 19445588PubMed |
López-Gresa MP, Torres C, Campos L, Lisón P, Rodrigo I, Bellés JM, Conejero V (2011) Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae. Environmental and Experimental Botany 74, 216–228.
| Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae.Crossref | GoogleScholarGoogle Scholar |
Ma Z, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Protection 24, 853–863.
| Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVCktLw%3D&md5=1043e9e38261a919c994491b80cea0b9CAS |
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262, 1432–1436.
| Map-based cloning of a protein kinase gene conferring disease resistance in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXpslekuw%3D%3D&md5=7851d9f0d7b74f0e594d1d13a3b76b9dCAS | 7902614PubMed |
Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology 138, 1083–1096.
| The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVejsLg%3D&md5=e886d7009c03c775861f27e5da23b802CAS | 15923334PubMed |
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology 51, 245–266.
| MAPK cascades in plant disease resistance signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOhtrvF&md5=1a1ad1fe729aead9c20877b3ba024823CAS | 23663002PubMed |
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628.
| Mapping and quantifying mammalian transcriptomes by RNA-Seq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnslyqs7k%3D&md5=e486628e6479f43aab29023bfba5b881CAS | 18516045PubMed |
Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Frontiers in Plant Science 6, 1–18.
| NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants.Crossref | GoogleScholarGoogle Scholar |
Nawrot R, Barylski J, Nowicki G, Broniarczyk J, Buchwald W, Goździcka-Józefiak A (2014) Plant antimicrobial peptides. Folia Microbiologica 59, 181–196.
| Plant antimicrobial peptides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFKjtrvN&md5=c36c789a43d21b86404cea216e1eea25CAS | 24092498PubMed |
Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56, 2907–2914.
| Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCjt7jJ&md5=27b1dae27b6b349786594192329c178bCAS | 16188960PubMed |
Par̆enicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis new openings to the MADS world. The Plant Cell 15, 1538–1551.
| Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis new openings to the MADS world.Crossref | GoogleScholarGoogle Scholar | 12837945PubMed |
Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489–521.
| Hormonal modulation of plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslagtbrE&md5=751ac331c523eacc3c7aa6bd3c958403CAS | 22559264PubMed |
Pluskal T, Castillo S, Villar-Briones A, Orešič M (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11, 1-11
| MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data.Crossref | GoogleScholarGoogle Scholar |
Prisic S, Xu M, Wilderman PR, Peters RJ (2004) Rice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions. Plant Physiology 136, 4228–4236.
| Rice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVartg%3D%3D&md5=48e1d4b33cffda0cb8be685b48184ab9CAS | 15542489PubMed |
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends in Plant Science 17, 369–381.
| NAC proteins: regulation and role in stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktlGltLw%3D&md5=918f476f0703b9fc8137387fda89ade4CAS | 22445067PubMed |
Pushpa D, Yogendra KN, Gunnaiah R, Kushalappa AC, Murphy A (2014) Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics. Plant Molecular Biology Reporter 32, 584–595.
| Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivF2jsLY%3D&md5=6f27986265d1ed1be3bccd43090f6437CAS |
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends in Plant Science 15, 247–258.
| WRKY transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVaqsbk%3D&md5=9dbc9b3ba5fcee35c634be9718264c5dCAS | 20304701PubMed |
Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nature Protocols 9, 2395–2410.
| Genome editing in rice and wheat using the CRISPR/Cas system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFOlu7fP&md5=c18c11c5c164bf45faa604951a013acfCAS | 25232936PubMed |
Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang CJ (2012) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Molecular Plant Pathology 13, 83–94.
| Rice WRKY45 plays important roles in fungal and bacterial disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCgu7o%3D&md5=d383a5847e7688cbb9a43d5eb156fc7dCAS | 21726399PubMed |
Singh B, Sharma RA (2015) Plant terpenes: defense responses, phylogenetic analysis, regulation and clinical applications. 3 Biotech 5, 129–151.
| Plant terpenes: defense responses, phylogenetic analysis, regulation and clinical applications.Crossref | GoogleScholarGoogle Scholar |
Song W-Y, Wang G-L, Chen L–L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhai W-X, Zhu L-H (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. science 270, 1804–1806.
| A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSiurnI&md5=af5db56263647424bfbabf45d7ec29eeCAS | 8525370PubMed |
Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie AR, Weisshaar B (2010) Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES‐dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11‐, MYB12‐and MYB111‐independent flavonol glycoside accumulation. New Phytologist 188, 985–1000.
| Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES‐dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11‐, MYB12‐and MYB111‐independent flavonol glycoside accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1arsL7J&md5=fbaf108dc1b445927937612afa4fe825CAS | 20731781PubMed |
Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. The Plant Journal 26, 101–112.
| The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1KlsL0%3D&md5=81d4994a1cb04a3f784f096cb79674ebCAS | 11359614PubMed |
The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475, 189–195.
| Genome sequence and analysis of the tuber crop potato.Crossref | GoogleScholarGoogle Scholar | 21743474PubMed |
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) mapman: a user‐driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914–939.
| mapman: a user‐driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFChu78%3D&md5=2fb16168e2beb41fade74ba13f698b43CAS | 14996223PubMed |
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111.
| TopHat: discovering splice junctions with RNA-Seq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWisrk%3D&md5=9e6dd93769d4a87bfd02a63b46b79413CAS | 19289445PubMed |
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511–515.
| Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVyitLY%3D&md5=353d41c250728a19a800b65fc219af3bCAS | 20436464PubMed |
Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environmental Chemistry Letters 4, 147–157.
| Significance of flavonoids in plant resistance: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFemsLvF&md5=9d92c60cbe37fc6412b969b2a84a5c78CAS |
Uhrig RG, Labandera A-M, Moorhead GB (2013) Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends in Plant Science 18, 505–513.
| Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslKqsrk%3D&md5=9512e76972e7299a9f7e67eaeb7bd580CAS | 23790269PubMed |
Usadel B, Poree F, Nagel A, Lohse M, Czedik Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare omics data in plants: a case study in the crop species, maize. Plant, Cell & Environment 32, 1211–1229.
| A guide to using MapMan to visualize and compare omics data in plants: a case study in the crop species, maize.Crossref | GoogleScholarGoogle Scholar |
Van Poppel PM, Jiang RH, Śliwka J, Govers F (2009) Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C‐terminal domains comprising W motifs. Molecular Plant Pathology 10, 611–620.
| Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C‐terminal domains comprising W motifs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFCgsbbN&md5=9dfdf677ad278dcc28741f077bfc3621CAS | 19694952PubMed |
Venisse J-S, Malnoy M, Faize M, Paulin J-P, Brisset M-N (2002) Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Molecular Plant-Microbe Interactions 15, 1204–1212.
| Modulation of defense responses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1Sjur8%3D&md5=7d04a8a08f5dc510b568fcafb373b1b6CAS | 12481992PubMed |
Yogendra KN, Pushpa D, Mosa KA, Kushalappa AC, Murphy A, Mosquera T (2014) Quantitative resistance in potato leaves to late blight associated with induced hydroxycinnamic acid amides. Functional & Integrative Genomics 14, 285–298.
| Quantitative resistance in potato leaves to late blight associated with induced hydroxycinnamic acid amides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVCmuw%3D%3D&md5=9077e9962c18d82a406a59ceae19cabfCAS |
Yogendra KN, Kumar A, Sarkar K, Li Y, Pushpa D, Mosa KA, Duggavathi R, Kushalappa AC (2015a) Transcription factor StWRKY1 regulates phenylpropanoid metabolites conferring late blight resistance in potato. Journal of Experimental Botany 66, 7377–7389.
| Transcription factor StWRKY1 regulates phenylpropanoid metabolites conferring late blight resistance in potato.Crossref | GoogleScholarGoogle Scholar | 26417019PubMed |
Yogendra KN, Kushalappa AC, Sarmiento F, Rodriguez E, Mosquera T (2015b) Metabolomics deciphers quantitative resistance mechanisms in diploid potato clones against late blight. Functional Plant Biology 42, 284–298.
Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. The Plant Cell 20, 2763–2782.
| A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWms7bF&md5=1af33789c7ca563b0f69e4b3dfe1825aCAS | 18952777PubMed |
Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, Xing Y, Zhang B, Liu H, Fengler KA (2015) A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics 47, 151–157.
| A maize wall-associated kinase confers quantitative resistance to head smut.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFKltL%2FP&md5=8409d2447bdb388c58b68588486713f9CAS | 25531751PubMed |
