Root-knot nematodes induce gall formation by recruiting developmental pathways of post-embryonic organogenesis and regeneration to promote transient pluripotency.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
07 2020
Historique:
received: 28 10 2019
accepted: 18 02 2020
pubmed: 5 3 2020
medline: 15 5 2021
entrez: 5 3 2020
Statut: ppublish

Résumé

Root-knot nematodes (RKNs; Meloidogyne spp.) induce new post-embryogenic organs within the roots (galls) where they stablish and differentiate nematode feeding cells, giant cells (GCs). The developmental programmes and functional genes involved remain poorly defined. Arabidopsis root apical meristem (RAM), lateral root (LR) and callus marker lines, SHORT-ROOT/SHR, SCARECROW/SCR, SCHIZORIZA/SCZ, WUSCHEL-RELATED-HOMEOBOX-5/WOX5, AUXIN-RESPONSIVE-FACTOR-5/ARF5, ARABIDOPSIS-HISTIDINE PHOSPHOTRANSFER-PROTEIN-6/AHP6, GATA-TRANSCRIPTION FACTOR-23/GATA23 and S-PHASE-KINASE-ASSOCIATED-PROTEIN2B/SKP2B, were analysed for nematode-dependent expression. Their corresponding loss-of-function lines, including those for LR upstream regulators, SOLITARY ROOT/SLR/IAA14, BONDELOS/BDL/IAA12 and INDOLE-3-ACETIC-ACID-INDUCIBLE-28/IAA28, were tested for RKN resistance/tolerance. LR genes, for example ARF5 (key factor for root stem-cell niche regeneration), GATA23 (which specifies pluripotent founder cells) and AHP6 (cytokinin-signalling-inhibitor regulating pericycle cell-divisions orientation), show a crucial function during gall formation. RKNs do not compromise the number of founder cells or LR primordia but locally induce gall formation possibly by tuning the auxin/cytokinin balance in which AHP6 might be necessary. Key RAM marker genes were induced and functional in galls. Therefore, the activation of plant developmental programmes promoting transient-pluripotency/stemness leads to the generation of quiescent-centre and meristematic-like cell identities within the vascular cylinder of galls. Nematodes enlist developmental pathways of new organogenesis and/or root regeneration in the vascular cells of galls. This should determine meristematic cell identities with sufficient transient pluripotency for gall organogenesis.

Identifiants

pubmed: 32129890
doi: 10.1111/nph.16521
doi:

Substances chimiques

Arabidopsis Proteins 0
Cytokinins 0
Indoleacetic Acids 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

200-215

Informations de copyright

© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.

Références

Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D. 2009. Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. The Plant Journal 57: 626-644.
Baldacci-Cresp F, Sacre PY, Twyffels L, Mol A, Vermeersch M, Ziemons E, Hubert P, Perez-Morga D, El Jaziri M, de Almeida Engler J et al. 2016. Poplar-root knot nematode interaction: a model for perennial woody species. Molecular Plant-Microbe Interactions 29: 560-572.
Barcala M, García A, Cabrera J, Casson S, Lindsey K, Favery B, García-Casado G, Solano R, Fenoll C, Escobar C. 2010. Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. The Plant Journal 61: 698-712.
Barcala M, García A, Cubas P, Almoguera C, Jordano J, Fenoll C, Escobar C. 2008. Distinct heat-shock element arrangements that mediate the heat shock, but not the late-embryogenesis induction of small heat-shock proteins, correlate with promoter activation in root-knot nematode feeding cells. Plant Molecular Biology 66: 151-164.
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA. 1993. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119: 57-70.
Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G, Chambrier P, Rozier F, Mirabet V, Legrand J, Laine S et al. 2014. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505: 417-421.
Beziat C, Kleine-Vehn J, Feraru E. 2017. Histochemical staining of beta-glucuronidase and its spatial quantification. In: Kleine-Vehn J, Sauer M, eds. Plant hormones. Methods in molecular biology. New York, NY, USA: Humana Press, 73-80.
Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN. 2007. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806.
Cabrera J, Barcala M, García A, Rio-Machín A, Medina C, Jaubert-Possamai S, Favery B, Maizel A, Ruiz-Ferrer V, Fenoll C et al. 2016. Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS 3-derived tasiRNAs. New Phytologist 209: 1625-1640.
Cabrera J, Díaz-Manzano FE, Sanchez M, Rosso M-N, Melillo T, Goh T, Fukaki H, Cabello S, Hofmann J, Fenoll C et al. 2014. A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis-Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytologist 203: 632-645.
Cabrera J, Fenoll C, Escobar C. 2015. Genes co-regulated with LBD16 in nematode feeding sites inferred from in silico analysis show similarities to regulatory circuits mediated by the auxin/cytokinin balance in Arabidopsis. Plant Signaling & Behavior 10: e990825.
Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735-743.
D'Agostino IB, Deruère J, Kieber JJ. 2000. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiology 124: 1706-1717.
Dastidar MG, Jouannet V, Maizel A. 2012. Root branching: mechanisms, robustness, and plasticity. Wiley Interdisciplinary Reviews: Developmental Biology 1: 329-343.
De Meutter J, Tytgat T, Prinsen E, Gheysen G, Van Onckelen H, Gheysen G. 2005. Production of auxin and related compounds by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Communications in Agricultural and Applied Biological Sciences 70: 51-60.
De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S. 2010. A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Current Biology 20: 1697-1706.
De Smet I, Lau S, Voß U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W. 2010. Bimodular auxin response controls organogenesis in Arabidopsis. Proceedings of the National Academy of Sciences, USA 107: 2705-2710.
Della Rovere F, Fattorini L, D'Angeli S, Veloccia A, Falasca G, Altamura MM. 2013. Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of Arabidopsis. Annals of Botany 112: 1395-1407.
Díaz-Manzano FE, Barcala M, Engler G, Fenoll C, de Almeida-Engler J, Escobar C. 2016a. A reliable protocol for in situ microRNAs detection in feeding sites induced by root-knot nematodes. Frontiers in Plant Science 7: 966.
Diaz-Manzano FE, Cabrera J, Ripoll JJ, Del Olmo I, Andres MF, Silva AC, Barcala M, Sanchez M, Ruiz-Ferrer V, de Almeida-Engler J et al. 2018. A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (miRNA172/TOE1/FT) in the feeding sites induced by Meloidogyne javanica in Arabidopsis thaliana. New Phytologist 217: 813-827.
Diaz-Manzano FE, Olmo R, Cabrera J, Barcala M, Escobar C, Fenoll C. 2016b. Long-term in vitro system for maintenance and amplification of root-knot nematodes in Cucumis sativus roots. Frontiers in Plant Science 7: 124.
DiDonato RJ, Arbuckle E, Buker S, Sheets J, Tobar J, Totong R, Grisafi P, Fink GR, Celenza JL. 2004. Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. The Plant Journal 37: 340-353.
Du Y, Scheres B. 2017. PLETHORA transcription factors orchestrate de novo organ patterning during Arabidopsis lateral root outgrowth. Proceedings of the National Academy of Sciences, USA 114: 11709-11714.
Efroni I, Mello A, Nawy T, Ip P-L, Rahni R, DelRose N, Powers A, Satija R, Birnbaum KD. 2016. Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165: 1721-1733.
Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C. 2003. Induction of the Hahsp17.7G4 promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant cells. Molecular Plant-Microbe Interactions 16: 1062-1068.
Fan M, Xu C, Xu K, Hu Y. 2012. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Research 22: 1169-1180.
Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M. 2005. Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. The Plant Journal 44: 382-395.
Gallagher KL, Paquette AJ, Nakajima K, Benfey PN. 2004. Mechanisms regulating SHORT-ROOT intercellular movement. Current Biology 14: 1847-1851.
Goh T, Joi S, Mimura T, Fukaki H. 2012. The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins. Development 139: 883-893.
Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G. 2008. A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiology 148: 358-368.
Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C. 2009. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21: 3119-3132.
Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novak O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G et al. 2012. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24: 2515-2527.
Hayashi K, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H. 2008. Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proceedings of the National Academy of Sciences, USA 105: 5632-5637.
Heyman J, Cools T, Canher B, Shavialenka S, Traas J, Vercauteren I, Van den Daele H, Persiau G, De Jaeger G, Sugimoto K. 2016. The heterodimeric transcription factor complex ERF115-PAT1 grants regeneration competence. Nature Plants 2: 16165.
ten Hove CA, Willemsen V, de Vries WJ, van Dijken A, Scheres B, Heidstra R. 2010. SCHIZORIZA encodes a nuclear factor regulating asymmetry of stem cell divisions in the Arabidopsis root. Current Biology 20: 452-457.
Ikeuchi M, Favero DS, Sakamoto Y, Iwase A, Coleman D, Rymen B, Sugimoto K. 2019. Molecular mechanisms of plant regeneration. Annual Review of Plant Biology 70: 377-406.
Ikeuchi M, Iwase A, Rymen B, Lambolez A, Kojima M, Takebayashi Y, Sakakibara H. 2017. Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiology 1753: 1158-1174.
Ikeuchi M, Sugimoto K, Iwase A. 2013. Plant callus: mechanisms of induction and repression. The Plant Cell 25: 3159-3173.
Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K et al. 2011. The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Current Biology 21: 508-514.
Karczmarek A, Overmars H, Helder J, Goverse A. 2004. Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Molecular Plant Pathology 5: 343-346.
Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH. 2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345: 808-811.
Kyndt T, Goverse A, Haegeman A, Warmerdam S, Wanjau C, Jahani M, Engler G, de Almeida Engler J, Gheysen G. 2016. Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes. Journal of Experimental Botany 67: 4559-4570.
Lee HW, Kim NY, Lee DJ, Kim J. 2009. LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiology 151: 1377-1389.
Liu J, Hu X, Qin P, Prasad K, Hu Y, Xu L. 2018. The WOX11-LBD16 pathway promotes pluripotency acquisition in callus cells during de novo shoot regeneration in tissue culture. Plant & Cell Physiology 59: 734-743.
Liu W, Yu J, Ge Y, Qin P, Xu L. 2018. Pivotal role of LBD16 in root and root-like organ initiation. Cellular and Molecular Life Sciences 75: 3329-3338.
Lucas M, Kenobi K, von Wangenheim D, Vobeta U, Swarup K, De Smet I, Van Damme D, Lawrence T, Peret B, Moscardi E et al. 2013. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proceedings of the National Academy of Sciences, USA 110: 5229-5234.
Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y. 2006. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94-98.
Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, De Rybel B, Beeckman T, Casero P, Gutierrez C, del Pozo JC. 2012. Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiology 160: 749-762.
Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ. 2003. Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Molecular Biology 53: 513-530.
Melnyk CW, Schuster C, Leyser O, Meyerowitz EM. 2015. A developmental framework for graft formation and vascular reconnection in Arabidopsis thaliana. Current Biology 25: 1306-1318.
Morales-Navarro S, Perez-Diaz R, Ortega A, de Marcos A, Mena M, Fenoll C, Gonzalez-Villanueva E, Ruiz-Lara S. 2018. Overexpression of a SDD1-like gene from wild tomato decreases stomatal density and enhances dehydration avoidance in Arabidopsis and cultivated tomato. Frontiers in Plant Science 9: 940.
Moreira S, Bishopp A, Carvalho H, Campilho A. 2013. AHP6 inhibits cytokinin signaling to regulate the orientation of pericycle cell division during lateral root initiation. PLoS ONE 8: e56370.
Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN. 2010. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306-1311.
Motte H, Vanneste S, Beeckman T. 2019. Molecular and environmental regulation of root development. Annual Review of Plant Biology 70: 465-488.
Mylona P, Linstead P, Martienssen R, Dolan L. 2002. SCHIZORIZA controls an asymmetric cell division and restricts epidermal identity in the Arabidopsis root. Development 129: 4327-4334.
Nakajima K, Sena G, Nawy T, Benfey PN. 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413: 307-311.
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19: 118-130.
Olmo R, Cabrera J, Fenoll C, Escobar C. 2019. A role for ALF4 during gall and giant cell development in the biotic interaction between Arabidopsis and Meloidogyne spp. Physiologia Plantarum 165: 17-28.
Olmo R, Cabrera J, Moreno-Risueno MA, Fukaki H, Fenoll C, Escobar C. 2017a. Molecular transducers from roots are triggered in Arabidopsis leaves by root-knot nematodes for successful feeding site formation: a conserved post-embryogenic de novo organogenesis program? Frontiers in Plant Science 8: 875.
Olmo R, Silva AC, Díaz-Manzano FE, Cabrera J, Fenoll C, Escobar C. 2017b. A standardized method to assess infection rates of root-knot and cyst nematodes in Arabidopsis thaliana mutants with alterations in root development related to auxin and cytokinin signaling. In: Dandekar T, Naseem M, eds. Auxins and cytokinins in plant biology. Methods in molecular biology. New York, NY, USA: Humana Press, 73-81.
Oshima Y, Mitsuda N, Nakata M, Nakagawa T, Nagaya S, Kato K, Ohme-Takagi M. 2011. Novel vector systems to accelerate functional analysis of transcription factors using chimeric repressor gene-silencing technology CRES-T. Plant Biotechnology 28: 201-210.
Ossowski S, Schwab R, Weigel D. 2008. Gene silencing in plants using artificial microRNAs and other small RNAs. The Plant Journal 53: 674-690.
Pernas M, Ryan E, Dolan L. 2010. SCHIZORIZA controls tissue system complexity in plants. Current Biology 20: 818-823.
Rodiuc N, Vieira P, Banora MY, de Almeida Engler J. 2014. On the track of transfer cell formation by specialized plant-parasitic nematodes. Frontiers in Plant Science 5: 160.
Sabatini S, Heidstra R, Wildwater M, Scheres B. 2003. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes & Development 17: 354-358.
Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464: 913-916.
Shang B, Xu C, Zhang X, Cao H, Xin W, Hu Y. 2016. Very-long-chain fatty acids restrict regeneration capacity by confining pericycle competence for callus formation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 113: 5101-5106.
Sugimoto K, Jiao Y, Meyerowitz EM. 2010. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Developmental Cell 18: 463-471.
Tellmann G. 2006. The E-Method: a highly accurate technique for gene expressionanalysis. Nature Methods 3: i-ii.
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. 1997. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
Wyss U, Grundler F, Munch A. 1992. The parasitic behaviour of second-stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica 38: 98-111.
Yamaguchi YL, Suzuki R, Cabrera J, Nakagami S, Sagara T, Ejima C, Sano R, Aoki Y, Olmo R, Kurata T et al. 2017. Root-knot and cyst nematodes activate procambium-associated genes in Arabidopsis roots. Frontiers in Plant Science 8: 1195.
Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B. 2019. A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177: 942-956.
Zuo J, Niu QW, Chua NH. 2000. Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. The Plant Journal 24: 265-273.

Auteurs

Rocío Olmo (R)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

Javier Cabrera (J)

Centro de Biotecnología y Genómica de Plantas (CBGP), Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus de Montegancedo, Pozuelo de Alarcón, 28223, Madrid, Spain.

Fernando E Díaz-Manzano (FE)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

Virginia Ruiz-Ferrer (V)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

Marta Barcala (M)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

Takashi Ishida (T)

International Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, 860-8555, Japan.

Alejandra García (A)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

María Fe Andrés (MF)

Protección Vegetal, Instituto de Ciencias Agrarias (ICA, CSIC), Calle de Serrano 115, 28006, Madrid, Spain.

Simón Ruiz-Lara (S)

Laboratorio de Genómica Funcional, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, 3460000, Chile.

Isabel Verdugo (I)

Laboratorio de Genómica Funcional, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, 3460000, Chile.

Mónica Pernas (M)

Centro de Biotecnología y Genómica de Plantas (CBGP), Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus de Montegancedo, Pozuelo de Alarcón, 28223, Madrid, Spain.

Hidehiro Fukaki (H)

Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodai, Kobe, 657-8501, Japan.

Juan Carlos Del Pozo (JC)

Centro de Biotecnología y Genómica de Plantas (CBGP), Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus de Montegancedo, Pozuelo de Alarcón, 28223, Madrid, Spain.

Miguel Ángel Moreno-Risueno (MÁ)

Centro de Biotecnología y Genómica de Plantas (CBGP), Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus de Montegancedo, Pozuelo de Alarcón, 28223, Madrid, Spain.

Tina Kyndt (T)

Department of Molecular Biotechnology, Ghent University, 9000, Ghent, Belgium.

Godelieve Gheysen (G)

Department of Molecular Biotechnology, Ghent University, 9000, Ghent, Belgium.

Carmen Fenoll (C)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.

Shinichiro Sawa (S)

International Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, 860-8555, Japan.

Carolina Escobar (C)

Facultad de Ciencias Ambientales y Bioquímica, Área de Fisiología Vegetal, Universidad de Castilla-La Mancha, Avda. Carlos III, s/n, 45071, Toledo, Spain.
International Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, 860-8555, Japan.

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