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Verticillium longisporum (Vl43) is a soilborne hemibiotrophic fungal pathogen causing stem striping on oilseed rape (OSR) and severe yield losses. Breeding for resistant varieties is the most promising approach to control this disease. Here, we report the identification of Hva22c as a novel susceptibility factor and its potential for improving OSR resistance. Hva22c is a member of the Hva22 gene family, originally described for barley (Hordeum vulgare). Several Hva22 members have been located at the endoplasmic reticulum. Hva22c is up-regulated in response to Vl43 in both Arabidopsis and OSR. We demonstrate that knock-out of Hva22c in OSR by CRISPR/Cas9 and its homolog in Arabidopsis by T-DNA insertion reduced plants’ susceptibility toVl43infection and impaired the development of disease symptoms. To understand the underlying mechanism, we analysed transcriptomic data from infected and non-infected roots of hva22c knock-out and wild type plants. We identified a homozygous mutant with frame-shifts in all four BnHva22c loci displaying a vastly altered transcriptional landscape at 6 dpi. Significantly, a large set of genes was suppressed under mock conditions including genes related to the endomembrane systems. Among the up-regulated genes we found several defense-related and phytohormone-responsive genes when comparing mutant to the wild type. These results demonstrate that Hva22c is functionally required for a fully compatible plant-fungus interaction. Its loss of function reduces plant susceptibility, most likely due to endoplasmatic reticulum and Golgi dysfunction accompanied by additionally activated defense responses. These findings can help improve OSR resistance to V. longisporum infection.
Y. Wang, S.E. Strelkov, S.F. Hwang, Blackleg yield losses and interactions with verticillium stripe in canola (Brassica napus) in Canada, Plants 12 (2023) 434.
M. Vega-Marin, A. von Tiedemann, Contrasting interactions of the aggressive Verticillium longisporum lineage A1/D1 and the non-aggressive A1/D2 lineage with roots of oilseed rape, Plant Pathol. 72 (2023) 1662–1672.
B. Chalhoub, F. Denoeud, S. Liu, I.A.P. Parkin, H. Tang, Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome, Science 354 (2014) 950–953.
D. Hu, W. Zhang, Y. Zhang, S. Chang, L. Chen, Y. Chen, Y. Shi, J. Shen, J. Meng, J. Zou, Reconstituting the genome of a young allopolyploid crop, Brassica napus, with its related species, Plant Biotechnol. J. 17 (2019) 1106–1118.
J.R. Depotter, S. Deketelaere, P. Inderbitzin, A. von Tiedemann, Verticillium longisporum, the invisible threat to oilseed rape and other brassicaceous plant hosts, Mol. Plant Pathol. 17 (2016) 1014–1016.
D. Schenke, D. Cai, Applications of CRISPR/Cas to improve crop disease resistance: beyond inactivation of susceptibility factors, iScience 23 (2020) 101478.
M. Pröbsting, D. Schenke, R. Hossain, C. Häder, T. Thurau, L. Wighardt, A. Schuster, Z. Zhou, Loss-of-function of CRT1a (calreticulin) reduces susceptibility to verticillium longisporum in both Arabidopsis thaliana and oilseed rape (Brassica napus), Plant Biotechnol. J. 18 (2020) 2328–2344.
Q. Shen, S.J. Uknes, T.H.D. Ho, Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene, J. Biol. Chem. 268 (1993) 23652–23660.
Q. Shen, C.N. Chen, A. Brands, S.M. Pan, T.H.D. Ho, The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms, Plant Mol. Biol. 45 (2001) 327–340.
W.J. Guo, T.H.D. Ho, An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells, Plant Physiol. 147 (2008) 1710–1722.
L. Fernandez-Calvino, C. Faulkner, J. Walshaw, G. Saalbach, E. Bayer, Y. Benitez-Alfonso, A. Maule, Arabidopsis plasmodesmal proteome, PLoS ONE 6 (2011) e18880.
P.L. Lu, Physiological functional analysis of a stress-induced protein, HVA22, in Escherichia coli, Int. J. Biol. Res. 1 (2013) 14–23.
A.H. Wai, M. Waseem, L.H. Cho, S.T. Kim, D.J. Lee, C.K. Kim, M.Y. Chung, Comprehensive genome-wide analysis and expression pattern profiling of the SlHVA22 gene family unravels their likely involvement in the abiotic stress adaptation of tomato, Int. J. Mol. Sci. 23 (2022), https://doi.org/10.3390/ijms232012222.
M.D. Gomes Ferreira, J. Araújo Castro, R.J. Santana Silva, F. Micheli, HVA22 from citrus: a small gene family whose some members are involved in plant response to abiotic stress, Plant Physiol. Biochem. 142 (2019) 395–404.
F. Meng, Q. Zhao, X. Zhao, C. Yang, R. Liu, J. Pang, W. Zhao, Q. Wang, M. Liu, Z. Zhang, Z. Kong, J. Liu, A rice protein modulates endoplasmic reticulum homeostasis and coordinates with a transcription factor to initiate blast disease resistance, Cell Rep. 39 (2022), https://doi.org/10.1016/j.celrep.2022.110941.
H. Zhang, Y. Yuan, H. Xing, M. Xin, M. Saeed, Q. Wu, J. Wu, T. Zhuang, X. Zhang, L. Mao, X. Sun, X. Song, Z. Wang, Genome-wide identification and expression analysis of the HVA22 gene family in cotton and functional analysis of GhHVA22E1D in drought and salt tolerance, Front. Plant Sci. 14 (2023) 1139526.
S.J. Clough, A.F. Bent, Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana, Plant J. 16 (1998) 735–743.
C. Eynck, B. Koopmann, G. Grunewald-Stoecker, P. Karlovsky, A. von Tiedemann, Differential interactions of Verticillium longisporum and V. dahliae with Brassica napus detected with molecular and histological techniques, Eur. J. Plant Pathol. 118 (2007) 259–274.
F.H. Behrens, D. Schenke, R. Hossain, C. Häder, Y. Zhao, W. Zhu, D. Cai, Suppression of abscisic acid (ABA) biosynthesisat the early infection stage of verticillium longisporum in oilseed rape (Brassica napus), Mol. Plant Pathol. 12867 (2019).
S.O. Rogers, A.J. Bendich, Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues, Plant Mol. Biol. 5 (1985) 69–76.
K. Tamura, G. Stecher, D. Peterson, A. Filipski, S. Kumar, MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol. 30 (2013) 2725–2729.
T. Hruz, O. Laule, G. Szabo, F. Wessendorp, S. Bleuler, L. Oertle, P. Widmayer, W. Gruissem, P. Zimmermann, Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes, Adv. Bioinformatics (2008) 420747.
J. Park, S. Bae, J.S. Kim, Cas-designer: a web-based tool for choice of CRISPR-Cas9 target sites, Bioinformatics 31 (2015) 4014–4016.
S. Bae, J. Park, J.S. Kim, Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNA-guided endonucleases, Bioinformatics 30 (2014) 1473–1475.
J.F. Li, J.E. Norville, J. Aach, M. McCormack, D. Zhang, J. Bush, G.M. Church, J. Sheen, Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9, Nat. Biotechnol. 31 (2013) 688–691.
S. Schiml, F. Fauser, H. Puchta, The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny, Plant J. 80 (2014) 1139–1150.
T. Nakagawa, T. Suzuki, S. Murata, S. Nakamura, T. Hino, K. Maeo, R. Tabata, T. Kawai, K. Tanaka, Y. Niwa, Y. Watanabe, K. Nakamura, T. Kimura, S. Ishiguro, Improved gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants, Biosci. Biotechnol. Biochem. 71 (2007) 2095–2100.
M.M. Neff, J.D. Nef, J. Chory, A.E. Pepperd, CAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics, Plant J. 14 (1998) 387–392.
C. Hodgens, Z.L. Nimchuk, J.J. Kieber, indCAPS: a tool for designing screening primers for CRISPR/Cas9 mutagenesis events, PLoS ONE 12 (2017) e0188406.
G. Yu, L.G. Wang, Y. Han, Q.Y. He, ClusterProfiler: an R package for comparing biological themes among gene clusters, OMICS 16 (2012) 284–287.
C.N. Chen, C.C. Chu, R. Zentella, S.M. Pan, T.H.D. Ho, AtHVA22 gene family in Arabidopsis: phylogenetic relationship, ABA and stress regulation, and tissuespecific expression, Plant Mol. Biol. 49 (2002) 633–644.
C.J. Park, J.M. Park, Endoplasmic reticulum plays a critical role in integrating signals generated by both biotic and abiotic stress in plants, Front. Plant Sci. 1 (2019) 399.
S.F. Zhou, L. Sun, A.E. Valdés, P. Engström, Z.T. Song, S.J. Lu, J.X. Liu, Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis, New Phytol. 208 (2015) 188–197.
Y.G. Yang, W.T. Lv, M.J. Li, B. Wang, D.M. Sun, X. Deng, Maize membrane-bound transcription factor Zmbzip17 is a key regulator in the cross-talk of ER quality control and ABA signaling, Plant Cell Physiol. 54 (2013) 2020–2033.
Y. Bao, S.H. Howell, The unfolded protein response supports plant development and defense as well as responses to abiotic stress, Front. Plant Sci. 8 (2017) 344.
J. Chen, G. Stefano, F. Brandizzi, H.Q. Zheng, Arabidopsis RHD3 mediates the generation of the tubular ER network and is required for golgi distribution and motility in plant cells, J. Cell Sci. 124 (2011) 2241–2252.
J.J. Hu, Y. Shibata, C. Voss, T. Shemesh, Z.L. Li, M. Coughlin, M.M. Kozlov, T.A. Rapoport, W.A. Prinz, Membrane proteins of the endoplasmic reticulum induce high-curvature tubules, Science 319 (2008) 1247–1250.
A. Wu, A.D. Allu, P. Garapati, H. Siddiqui, H. Dortay, M.I. Zanor, M.A. Asensi-Fabado, S. Munné-Bosch, C. Antonio, T. Tohge, A.R. Fernie, K. Kaufmann, G.P. Xue, B. Mueller-Roeber, S. Balazadeh, JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis, Plant Cell 24 (2012) 482–506.
Z.T. Yang, S.J. Lu, M.J. Wang, D.L. Bi, L. Sun, S.F. Zhou, Z.T. Song, J.X. Liu, A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis, Plant J. 79 (2014) 1033–1043.
P.J. Seo, M.J. Kim, J.Y. Park, S.Y. Kim, J. Jeon, Y.H. Lee, J. Kim, C.M. Park, Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis, Plant J. 61 (2010) 661–671.
H. Peng, J. Phung, E.C. Stowe, A. Dhingra, M.M. Neff, The NAC transcription factor ATAF2 promotes ethylene biosynthesis and response in Arabidopsis thaliana seedlings, FEBS Lett. 596 (2022) 1586–1599.
C. Delessert, K. Kazan, I.W. Wilson, D. Van Der Straeten, J. Manners, E.S. Dennis, R. Dolferus, The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis, Plant J. 43 (2005) 745–757.
H. McLellan, P.C. Boevink, M.R. Armstrong, L. Pritchard, S. Gomez, J. Morales, S.C. Whisson, J.L. Beynon, P.R. Birch, An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus, PLoS Pathol. 9 (2013) e1003670.
L. Liu, L. Qin, L.B. Safdar, C. Zhao, X. Cheng, M. Xie, Y. Zhang, F. Gao, Z. Bai, J. Huang, R.P. Bhalerao, S. Liu, Y. Wei, The plant trans-golgi network component ECHIDNA regulates defense, cell death, and endoplasmic reticulum stress, Plant Physiol. 191 (2023) 558–574.
Q. Rui, X. Tan, F. Liu, Y. Bao, An update on the key factors required for plant golgi structure maintenance, Front. Plant Sci. 13 (2022) 933283.
L. Elliott, I. Moore, C. Kirchhelle, Spatio-temporal control of post-golgi exocytic trafficking in plants, J. Cell Sci. 133 (2020) 933283.
D. Schenke, D. Cai, Phytohormone crosstalk in the host-verticillium interaction, Plant Signal. Behav. 15 (2020) e1803567.
D. Schenke, K. Naito, K. Toyoda, Y. Inagaki, T. Shiraishi, Y. Ichinose, Regulation of elicitin-induced ethylene production in suspension cultured tobacco BY-2 cells, J. Gen. Plant Pathol. 71 (2005) 273–279.
D.R. Gallie, Ethylene receptors in plants - why so much complexity? F1000prime Rep. 7 (2015) 39.
Z. Zhu, B. Lee, Friends or foes: new insights in jasmonate and ethylene co-actions, Plant Cell Physiol. 56 (2015) 414–420.
A.J. Koo, C. Thireault, S. Zemelis, A.N. Poudel, T. Zhang, N. Kitaoka, F. Brandizzi, H. Matsuura, G.A. Howe, Endoplasmic reticulum-associated inactivation of the hormone jasmonoyl-L-isoleucine by multiple members of the cytochrome P450 94 family in Arabidopsis, J. Biol. Chem. 289 (2014) 29728–29738.
J. Wu, A.M. van der Burgh, G. Bi, L. Zhang, J.R. Alfano, G.B. Martin, M.H.A.J. Joosten, The bacterial effector AvrPto targets the regulatory coreceptor SOBIR1 and suppresses defense signaling mediated by the receptor-like protein Cf-4, Mol. Plant-Microbe Interact. 31 (2018) 75–85.
S. Rietz, F.E. Bernsdorff, D. Cai, Members of the germin-like protein family in Brassica napus are candidates for the initiation of an oxidative burst that impedes pathogenesis of Sclerotinia sclerotiorum, J. Exp. Bot. 63 (2012) 5507–5519.
M.L. Falcone Ferreyra, J. Emiliani, E.J. Rodriguez, V.A. Campos-Bermudez, E. Grotewold, P. Casati, The identification of maize and Arabidopsis type I FLAVONE SYNTHASEs links flavones with hormones and biotic Interactions, Plant Physiol. 169 (2015) 1090–1107.
M. van Damme, R.P. Huibers, J. Elberse, G. van den Ackerveken, Arabidopsis DMR6 encodes a putative 2OG-fe (Ⅱ) oxygenase that is defense-associated but required for susceptibility to downy mildew, Plant J. 54 (2008) 785–793.
D.P.T. Thomazella, K. Seong, R. Mackelprang, D. Dahlbeck, Y. Geng, U.S. Gill, T. Qi, J. Pham, P. Giuseppe, C.Y. Lee, A. Ortega, M.J. Cho, S.F. Hutton, Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance, Proc. Natl. Acad. Sci. U. S. A. 118 (2021) e2026152118.
J.A.R. Hasley, N. Navet, M. Tian, CRISPR/Cas9-mediated mutagenesis of sweet basil candidate susceptibility gene ObDMR6 enhances downy mildew resistance, PLoS ONE 16 (2021) e0253245.
Y.C. Low, M.A. Lawton, R. Di, Validation of barley 2OGO gene as a functional orthologue of Arabidopsis DMR6 gene in Fusarium head blight susceptibility, Sci. Rep. 10 (2020) 9935.
J.N. Tripathi, V.O. Ntui, T. Shah, L. Tripathi, CRISPR/Cas9-mediated editing of DMR6 orthologue in banana (Musa spp.) confers enhanced resistance to bacterial disease, Plant Biotechnol. J. 19 (2021) 1291–1293.
V. Pavese, A. Moglia, P. Gonthier, D. Torello Marinoni, E. Cavalet-Giorsa, R. Botta, Identification of susceptibility genes in Casta nea sativa and their transcription dynamics following pathogen infection, Plants 10 (2021) 913.
N.P. Kieu, M. Lenman, E.S. Wang, B.L. Petersen, E. Andreasson, Mutations introduced in susceptibility genes through CRISPR/Cas9 genome editing confer increased late blight resistance in potatoes, Sci. Rep. 11 (2021) 4487.
L. Giacomelli, T. Zeilmaker, O. Giovannini, U. Salvagnin, D. Masuero, P. Franceschi, U. Vrhovsek, S. Scintilla, J. Rouppe van der Voort, C. Moser, Simultaneous editing of two DMR6 genes in grapevine results in reduced susceptibility to downy mildew, Front. Plant Sci. 14 (2023) 1242240.
S.S. Scholz, W. Schmidt-Heck, R. Guthke, A.C.U. Furch, M. Reichelt, J. Gershenzon, R. Oelmüller, Verticillium dahliae-Arabidopsis interaction causes changes in gene expression profiles and jasmonate levels on different time scales, Front. Microbiol. 9 (2018) 217.
J.L. Freeman, L.H. Zhang, M.A. Marcus, S. Fakra, S.P. McGrath, E.A. Pilon-Smits, Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata, Plant Physiol. 142 (2006) 124–134.
S. König, K. Feussner, A. Kaever, M. Landesfeind, C. Thurow, P. Karlovsky, C. Gatz, A. Polle, I. Feussner, Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum, New Phytol. 202 (2014) 823–837.
C. Obermeier, M.A. Hossain, R. Snowdon, J. Knuefer, A. von Tiedemann, W. Friedt, Genetic analysis of phenylpropanoid metabolites associated with resistance against Verticillium longisporum in Brassica napus, Mol. Breed. 31 (2013) 347–361.
S. Kusch, R. Panstruga, mlo-based resistance: an apparently universal ‘‘weapon” to defeat powdery mildew disease, Mol. Plant-Microbe Interact. 30 (2017) 179–189.
S. Li, D. Lin, Y. Zhang, M. Deng, Y. Chen, B. Lv, B. Li, Y. Lei, Y. Wang, L. Zhao, Y. Liang, J. Liu, K. Chen, Z. Liu, J. Xiao, J.L. Qiu, C. Gao, Genome-edited powdery mildew resistance in wheat without growth penalties, Nature 602 (2022) 455–460.
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