The Streamlined Genome of Phytomonas spp. Relative to Human Pathogenic Kinetoplastids Reveals a Parasite Tailored for Plants

Betina M Porcel,Sandrine Fabre,Jeremy C Mottram,Mark C Field,Patrick Wincker,Corinne Da Silva,Frédéric Bringaud,Michel Dollet,Tansy C Hammarton,Shulamit Michaeli,Roberto Docampo,Dan Zilberstein,David A Campbell,Balázs Szöőr,Julie Poulain,Nicholas J Dickens,Arnaud Couloux,Nancy R Sturm,Julius Lukeš,Pavel Flegontov,Kamel Jabbari,Benjamin Noël ,Michaël Katinka ,Frederik Opperdoes ,Roxana Cintrón ,Vassiliki Lila Koumandou ,Mohammed‐Amin Madoui ,Jean‐Marc Aury

doi:10.1371/journal.pgen.1004007

Abstract

Members of the family Trypanosomatidae infect many organisms, including animals, plants and humans. Plant-infecting trypanosomes are grouped under the single genus Phytomonas, failing to reflect the wide biological and pathological diversity of these protists. While some Phytomonas spp. multiply in the latex of plants, or in fruit or seeds without apparent pathogenicity, others colonize the phloem sap and afflict plants of substantial economic value, including the coffee tree, coconut and oil palms. Plant trypanosomes have not been studied extensively at the genome level, a major gap in understanding and controlling pathogenesis. We describe the genome sequences of two plant trypanosomatids, one pathogenic isolate from a Guianan coconut and one non-symptomatic isolate from Euphorbia collected in France. Although these parasites have extremely distinct pathogenic impacts, very few genes are unique to either, with the vast majority of genes shared by both isolates. Significantly, both Phytomonas spp. genomes consist essentially of single copy genes for the bulk of their metabolic enzymes, whereas other trypanosomatids e.g. Leishmania and Trypanosoma possess multiple paralogous genes or families. Indeed, comparison with other trypanosomatid genomes revealed a highly streamlined genome, encoding for a minimized metabolic system while conserving the major pathways, and with retention of a full complement of endomembrane organelles, but with no evidence for functional complexity. Identification of the metabolic genes of Phytomonas provides opportunities for establishing in vitro culturing of these fastidious parasites and new tools for the control of agricultural plant disease.

Highlights

Flagellated protists of the family Trypanosomatidae, class Kinetoplastea, infect a large variety of organisms including animals, plants and humans [1]
Single-celled organisms living in phloem sap, are responsible for important palm diseases, inducing frequent expensive and toxic insecticide treatments against their insect vectors
Despite the wide range of behaviors and impacts, these trypanosomes have been rather unceremoniously lumped into a single genus: Phytomonas

Summary

Introduction

Flagellated protists of the family Trypanosomatidae, class Kinetoplastea, infect a large variety of organisms including animals, plants and humans [1]. Filamentous microorganisms like oomycetes and fungi have acquired the capacity to infect and grow inside the plant tissues. While some of these organisms could influence plant growth positively, in most cases they can cause major diseases in plants of economic importance [5]. The genomes of numerous of these filamentous plant pathogens have already been sequenced, unveiling an amazing variety of genome sizes and organization [6]. Some filamentous plant pathogens have fairly small genomes, as a consequence of intron or gene loss, like U. maydis;(21 Mb) [7] and Albugo laibachii; (37 Mb) [8], or abridged transposon content as in Sclerotinia sclerotiorum; (38 Mb) [9]

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Conclusion