Xyloglucan processing machinery in Xanthomonas pathogens and its role in the transcriptional activation of virulence factors

P.S. Vieira(Brazilian Center for Research in Energy and Materials), Isabela Mendes Bonfim(Universidade Estadual de Campinas (UNICAMP)), Evandro Ares de Araújo(Brazilian Synchrotron Light Laboratory), Ricardo Rodrigues de Melo(Brazilian Center for Research in Energy and Materials), Augusto R. Lima(Brazilian Center for Research in Energy and Materials), Melissa Regina Fessel(Instituto Butantan), Maria Paula Paixão(Brazilian Center for Research in Energy and Materials), Gabriela Félix Persinoti(Brazilian Center for Research in Energy and Materials), Silvana A. Rocco(Brazilian Center for Research in Energy and Materials), Tatiani B. Lima(Brazilian Center for Research in Energy and Materials), Renan A. S. Pirolla(Brazilian Center for Research in Energy and Materials), M.A.B. Morais(Brazilian Center for Research in Energy and Materials), Jessica B. L. Correa(Brazilian Center for Research in Energy and Materials), L.M. Zanphorlin(Brazilian Center for Research in Energy and Materials), José Diogo(Universidade Estadual de Campinas (UNICAMP)), E.A. Lima(Brazilian Center for Research in Energy and Materials), Adriana Grandis(Universidade de São Paulo), Marcos Silveira Buckeridge(Universidade de São Paulo), Fábio C. Gozzo(Universidade Estadual de Campinas (UNICAMP)), Celso Eduardo Benedetti(Brazilian Center for Research in Energy and Materials), Igor Polikarpov(Universidade de São Paulo), P.O. Giuseppe(Brazilian Center for Research in Energy and Materials), M.T. Murakami(Brazilian Center for Research in Energy and Materials)
Nature Communications
June 30, 2021
Cited by 92Open Access
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Abstract

Xyloglucans are highly substituted and recalcitrant polysaccharides found in the primary cell walls of vascular plants, acting as a barrier against pathogens. Here, we reveal that the diverse and economically relevant Xanthomonas bacteria are endowed with a xyloglucan depolymerization machinery that is linked to pathogenesis. Using the citrus canker pathogen as a model organism, we show that this system encompasses distinctive glycoside hydrolases, a modular xyloglucan acetylesterase and specific membrane transporters, demonstrating that plant-associated bacteria employ distinct molecular strategies from commensal gut bacteria to cope with xyloglucans. Notably, the sugars released by this system elicit the expression of several key virulence factors, including the type III secretion system, a membrane-embedded apparatus to deliver effector proteins into the host cells. Together, these findings shed light on the molecular mechanisms underpinning the intricate enzymatic machinery of Xanthomonas to depolymerize xyloglucans and uncover a role for this system in signaling pathways driving pathogenesis.


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