Biotic Host–Pathogen Interactions As Major Drivers of Plastid Endosymbiosis. (April 2017)

• Record Type: Journal Article
• Authors: Cenci, Ugo; Bhattacharya, Debashish; Weber, Andreas P.M.; Colleoni, Christophe; Subtil, Agathe; Ball, Steven G.
• Is Part Of: Trends in plant science. Volume 22:Number 4(2017)
• Page Start: 316
• Page End: 328
• Publication Date: 2017-04
• Subjects: bacterial conjugation -- chlamydia -- evolution of plastids -- glycogen metabolism -- T3SS -- tryptophan synthesis; Botany -- Periodicals; Botanique -- Périodiques; Botany; Periodicals; 580.5
• DOI: 10.1016/j.tplants.2016.12.007
• Languages: English
• ISSNs: 1360-1385

Abstract

Abstract : The plastid originated 1.5 billion years ago through a primary endosymbiosis involving a heterotrophic eukaryote and an ancient cyanobacterium. Phylogenetic and biochemical evidence suggests that the incipient endosymbiont interacted with an obligate intracellular chlamydial pathogen that housed it in an inclusion. This aspect of the ménage-à- trois hypothesis (MATH) posits that Chlamydiales provided critical novel transporters and enzymes secreted by the pathogens in the host cytosol. This initiated the efflux of photosynthate to both the inclusion lumen and host cytosol. Here we review the experimental evidence supporting the MATH and focus on chlamydial genes that replaced existing cyanobacterial functions. The picture emerging from these studies underlines the importance of chlamydial host-pathogen interactions in the metabolic integration of the primary plastid. Trends: Phylogenetic analysis has detected over 50 lateral gene transfers shared between Chlamydiales and the ancestor of all photosynthetic eukaryotes. The ' ménage -à -trois hypothesis' proposes that Chlamydiales secreted enzymes required for assimilation of photosynthetic carbon in the cytosol of the eukaryote host of plastid endosymbiosis. Recent evidence suggests that the chlamydial genes involved in photosynthate export from the plastid were donated by conjugation in a common inclusion vacuole. Glycogen metabolism of extant Chlamydiaceae provides evidence that ancient Chlamydiales were preadapted to generate the carbohydrate flux detailed in the MATH. Analysis of tryptophan metabolism genes in plants suggests that the tryptophan metabolism operon of Chlamydiales was donated through conjugation to the evolving plastid genome to ensure tryptophan export to the inclusion.