Symptom evolution following the emergence of maize streak virus.

Adérito Luis Monjane ,Pierre Lefeuvre,Rizwan A Syed,Marion Bezuidenhout,Rémy Froissart,Arvind Varsani,Penelope Hartnady,Philippe Roumagnac,Simon Dellicour,Daphné Linderme,Elham Yazdkhasti,Anders Kvarnheden,Lara Donaldson,Philippe Lemey,Edward P Rybicki ,Betty E Owor ,Shane L Murray ,Gordon William Harkins ,Kehinde Adewole Oyeniran ,Dionne N Shepherd ,Marc A Suchard

doi:10.7554/elife.51984

Abstract

For pathogens infecting single host species evolutionary trade-offs have previously been demonstrated between pathogen-induced mortality rates and transmission rates. It remains unclear, however, how such trade-offs impact sub-lethal pathogen-inflicted damage, and whether these trade-offs even occur in broad host-range pathogens. Here, we examine changes over the past 110 years in symptoms induced in maize by the broad host-range pathogen, maize streak virus (MSV). Specifically, we use the quantified symptom intensities of cloned MSV isolates in differentially resistant maize genotypes to phylogenetically infer ancestral symptom intensities and check for phylogenetic signal associated with these symptom intensities. We show that whereas symptoms reflecting harm to the host have remained constant or decreased, there has been an increase in how extensively MSV colonizes the cells upon which transmission vectors feed. This demonstrates an evolutionary trade-off between amounts of pathogen-inflicted harm and how effectively viruses position themselves within plants to enable onward transmission.

Highlights

Maize was first introduced to Africa from South America in the early 1500s, and within 300 years became one of the most important food crops on the continent (McCann, 2001)
It is expected that pathogens like maize streak virus (MSV)-A will evolve over time to maximise their probability of transmission, there is a spectrum of possible ways in which this transmission optimisation imperative might impact the evolution of pathogen-mediated molecular processes that underlie infection symptoms (Bull and Lauring, 2014; Cressler et al, 2016; Doumayrou et al, 2013; Escriu et al, 2003; Mauck et al, 2010; Read, 1994)
What we find is that patterns of MSV-A symptom evolution over the last century are broadly consistent with there being a trade-off between transmission probabilities and the amount of harm MSV inflicts on infected maize

Summary

Introduction

Maize was first introduced to Africa from South America in the early 1500s, and within 300 years became one of the most important food crops on the continent (McCann, 2001). Whereas the spatial arrangements and dimensions of chlorotic lesions on MSV-infected maize leaves directly indicate the locations and numbers of leaf cells that are infected by MSV (Lucy, 1996), the colour of chlorotic streaks indicates the degree to which photosynthesis is impaired within infected cells (Pinner et al, 1993) Another quantifiable symptom of MSV infections that may impact the probability of virus transmission is leaf stunting. Whereas the intensity of chlorosis within streaks reflects the extent of chloroplast destruction within infected photosynthesising cells, it could be associated with the probability of onward MSV transmission This is because the sap-feeding insects that transmit viruses such as MSV tend to prefer pale-yellow over green when selecting feeding sites on leaves (Fereres and Moreno, 2009; Hodge and Powell, 2008; Isaacs et al, 1999). What we find is that patterns of MSV-A symptom evolution over the last century are broadly consistent with there being a trade-off between transmission probabilities and the amount of harm MSV inflicts on infected maize

Results and discussion

Materials and methods

Funding Funder Svenska Institutet