Identification of a molecular dialogue between developing seeds of Medicago truncatula and seedborne xanthomonads.
Plant pathogenic bacteria disseminate and survive mainly in association with seeds. This study addresses whether seeds are passive carriers or engage a molecular dialogue with pathogens during their development. We developed two pathosystems using Medicago truncatula with Xanthomonas alfalfae subsp. alfalfae (Xaa), the natural Medicago sp. pathogen and Xanthomonas campestris pv. campestris (Xcc), a Brassicaceae pathogen. Three days after flower inoculation, the transcriptome of Xcc-infected pods showed activation of an innate immune response that was strongly limited in Xcc mutated in the type three secretion system, demonstrating an incompatible interaction of Xcc with the reproductive structures. In contrast, the presence of Xaa did not result in an activation of defence genes. Transcriptome profiling during development of infected seeds exhibited time-dependent and differential responses to Xcc and Xaa. Gene network analysis revealed that the transcriptome of Xcc-infected seeds was mainly affected during seed filling whereas that of Xaa-infected seeds responded during late maturation. The Xcc-infected seed transcriptome exhibited an activation of defence response and a repression of targeted seed maturation pathways. Fifty-one percent of putative ABSCISIC ACID INSENSITIVE3 targets were deregulated by Xcc, including oleosin, cupin, legumin and chlorophyll degradation genes. At maturity, these seeds displayed decreased weight and increased chlorophyll content. In contrast, these traits were not affected by Xaa infection. These findings demonstrate the existence of a complex molecular dialogue between xanthomonads and developing seeds and provides insights into a previously unexplored trade-off between seed development and pathogen defence.
Université d'Angers, Institut de Recherche en Horticulture et Semences, UMR 1345, SFR 4207 QUASAV, 16 Boulevard Lavoisier, F-49045 Angers, France.
Emmanuel
E
Terrasson
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 42 rue Georges Morel, F-49071 Beaucouzé, France.
Armelle
A
Darrasse
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 16 Boulevard Lavoisier, F-49045 Angers.
Karima
K
Righetti
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 16 Boulevard Lavoisier, F-49045 Angers.
Julia
http://orcid.org/0000-0002-1457-764X
J
Buitink
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 16 Boulevard Lavoisier, F-49045 Angers.
David
D
Lalanne
Agrocampus Ouest, Institut de Recherche en Horticulture et Semences, UMR 1345, 49045 Angers, France.
Benoit
B
Ly Vu
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 16 Boulevard Lavoisier, F-49045 Angers.
Sandra
S
Pelletier
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 16 Boulevard Lavoisier, F-49045 Angers.
William
W
Bolingue
Institut National de la Recherche Agronomique, Institut de Recherche en Horticulture et Semences, UMR 1345, 42 rue Georges Morel, F-49071 Beaucouzé, France Marie-Agnes.Jacques@angers.inra.fr olivier.leprince@agrocampus-ouest.fr.
Marie-Agnès
MA
Jacques
Agrocampus Ouest, Institut de Recherche en Horticulture et Semences, UMR 1345, 49045 Angers, France Marie-Agnes.Jacques@angers.inra.fr olivier.leprince@agrocampus-ouest.fr.
Olivier
http://orcid.org/0000-0003-1414-8690
O
Leprince
D002734:Chlorophyll / Q000378:metabolism; D044127:Epigenesis, Genetic; D035264:Flowers / Q000382:microbiology; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D053263:Gene Regulatory Networks; D017343:Genes, Plant; D054884:Host-Pathogen Interactions / Q000235:genetics; D046913:Medicago truncatula / Q000196:embryology* / Q000235:genetics / Q000382:microbiology*; D009929:Organ Size; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D044945:Proanthocyanidins / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012098:Reproduction; D012639:Seeds / Q000196:embryology* / Q000235:genetics / Q000382:microbiology*; D013312:Stress, Physiological; D013997:Time Factors; D059467:Transcriptome / Q000235:genetics; D014974:Xanthomonas
D010940:Plant Proteins; D044945:Proanthocyanidins; D012333:RNA, Messenger; D002734:Chlorophyll; C013221:proanthocyanidin
ABI3; Medicago truncatula; Xanthomonas alfalfae; Xanthomonas campestris.; defence response; late embryogenesis abundant (LEA) genes; seed development; seed transmission