Abstract

Simultaneous infection of a single plant by various pathogen species is increasingly recognized as an important modulator of host resistance and a driver of pathogen evolution. Because plants in agro-ecosystems are the target of a multitude of pathogenic microbes, co-infection could be frequent, and consequently important to consider. This is particularly true for rapidly intensifying crops, such as rice in Africa. This study investigated potential interactions between pathogens causing two of the major rice diseases in Africa: the Rice yellow mottle virus (RYMV) and the bacterium Xanthomonas oryzae pathovar oryzicola (Xoc) in order to: 1/ document virus-bacteria co-infection in rice in the field, 2/ explore experimentally their consequences in terms of symptom development and pathogen multiplication, 3/ test the hypothesis of underlying molecular mechanisms of interactions and 4/ explore potential evolutionary consequences. Field surveys in Burkina Faso revealed that a significant proportion of rice fields were simultaneously affected by the two diseases. Co-infection leads to an increase in bacterial specific symptoms, while a decrease in viral load is observed compared to the mono-infected mock. The lack of effect found when using a bacterial mutant for an effector specifically inducing expression of a small RNA regulatory protein, HEN1, as well as a viral genotype-specific effect, both suggest a role for gene silencing mechanisms mediating the within-plant interaction between RYMV and Xoc. Potential implications for pathogen evolution could not be inferred because genotype-specific effects were found only for pathogens originating from different countries, and consequently not meeting in the agrosystem. We argue that pathogen-pathogen-host interactions certainly deserve more attention, both from a theoretical and applied point of view.

Highlights

  • Multiple Infections in Plant PathosystemsPlant pathologists have mostly focused on a tight pair of one plant-one pathogen interactions

  • There is accumulating evidence that various pathogen species or genotypes may coexist within a single plant in agro-ecosystems (Barrett et al, 2009; Lamichhane and Venturi, 2015; Tollenaere et al, 2016), a phenomenon hereafter defined as co-infection or multiple infections

  • Co-Occurrence of Rice yellow mottle virus (RYMV) and Xanthomonas oryzae pathovar oryzicola (Xoc) Reaches More Than 50% of the Fields in a Highly Infected Perimeter in Burkina Faso

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Summary

Introduction

Multiple Infections in Plant PathosystemsPlant pathologists have mostly focused on a tight pair of one plant-one pathogen interactions. During co-infection, the presence of co-infecting pathogens sharing the same host plant may affect the outcome of infection, both in terms of intra-host pathogen accumulation and symptom development (Tollenaere et al, 2016), as primarily reported for plant viruses (see for example Gil-Salas et al, 2012, and for a comprehensive review Syller, 2012), but was shown across different kingdoms (see for example Le May et al, 2009; Shapiro et al, 2013; Orton and Brown, 2016) when investigated Such pathogen-pathogen interactions may be direct or indirect and unpredictably synergistic or antagonistic (Tollenaere et al, 2016). These effects evidenced at individual plant levels may translate to the population level, with epidemiological (Zhang et al, 2001) and evolutionary (Alizon et al, 2013) consequences

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