Effects of virus infection on pollen production and pollen performance: Implications for the spread of resistance alleles

Harth, Jacquelyn E.; Winsor, James A.; Weakland, Danelle R.; Nowak, Kayla; Ferrari, Matthew J.; Stephenson, Andrew G.

doi:10.3732/ajb.1500165

Cited by 15 publications

(11 citation statements)

References 49 publications

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“…Overall plant growth was stunted by CMV infection ( S2 Fig ) but, interestingly, virus infection appeared to accelerate the appearance of flowers by a small but statistically significant degree ( S2 Fig ). A recent report indicated that flowers of squash ( Cucurbita pepo ) plants infected with the potyvirus zucchini yellow mosaic virus yielded decreased quantities of pollen [ 26 ]. However, we found no significant differences in the quantity or viability of pollen released from mock-inoculated and CMV-infected tomato flowers ( S3 Fig ).…”

Section: Resultsmentioning

confidence: 99%

Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?

et al. 2016

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Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by ‘buzzing’ (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts.

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Section: Resultsmentioning

confidence: 99%

Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?

et al. 2016

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“…We have extensively studied the interactions among pathogens and herbivores in populations of Cucurbita pepo ssp. texana (e.g., Hayes et al, 2004 ; Stephenson et al, 2004 ; Ferrari et al, 2007 ; Du et al, 2008 ; Sasu et al, 2009 , 2010a , b ; Simmons et al, 2011 ; Shapiro et al, 2012 , 2014 ; Harth et al, 2016 ) under laboratory, greenhouse and field conditions. Cucurbita pepo ssp.…”

Section: Introductionmentioning

confidence: 99%

Zucchini Yellow Mosaic Virus Infection Limits Establishment and Severity of Powdery Mildew in Wild Populations of Cucurbita pepo

et al. 2018

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Few studies have examined the combined effect of multiple parasites on host fitness. Previous work in the Cucurbita pepo pathosystem indicates that infection with Zucchini yellow mosaic virus (ZYMV) reduces exposure to a second insect-vectored parasite (Erwinia tracheiphila). In this study, we performed two large-scale field experiments employing wild gourds (Cucurbita pepo ssp. texana), including plants with a highly introgressed transgene conferring resistance to ZYMV, to examine the interaction of ZYMV and powdery mildew, a common fungal disease. We found that ZYMV-infected plants are more resistant to powdery mildew (i.e., less likely to experience powdery mildew infection and when infected with powdery mildew, have reduced severity of powdery mildew symptoms). As a consequence, during widespread viral epidemics, proportionally more transgenic plants get powdery mildew than non-transgenic plants, potentially mitigating the benefits of the transgene. A greenhouse study using ZYMV-inoculated and non-inoculated controls (non-transgenic plants) revealed that ZYMV-infected plants were more resistant to powdery mildew than controls, suggesting that the transgene itself had no direct effect on the powdery mildew resistance in our field study. Additionally, we found evidence of elevated levels of salicylic acid, a phytohormone that mediates anti-pathogen defenses, in ZYMV-infected plants, suggesting that viral infection induces a plant immune response (systemic acquired resistance), thereby reducing plant susceptibility to powdery mildew infection.

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“…Considerable evidence exists for wild radish (Marshall et al, 2010) and for other species (Rao et al, 1992; Havens et al, 1995; Demchik and Day, 1996; Agrawal et al, 1999; Lehtilä and Strauss, 1999; Galen, 2000; Pendleton, 2000; Galloway, 2001; Poulton et al, 2001a, b, 2002; Etterson and Galloway, 2002; Avila‐Sakar et al, 2003; Galen and Stanton, 2003; Hedhly et al, 2005) that environmental conditions for the pollen donor affect pollen and pollen tube quality. Generally, pollen donors grown under low water or low nutrients, exposed to herbivory, or affected by pathogens sire fewer seeds (Young and Stanton, 1990a; Lau and Stephenson, 1993; Quesada et al, 1995; Poulton et al, 2001b; Strauss et al, 2001; Pasonen et al, 2002; Hersch, 2006; Harth et al, 2016, in this issue). During our experiment, plants were used both as pollen donors and pollen recipients.…”

Section: Discussionmentioning

confidence: 99%

Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, Raphanus sativus

Marshall

Evans

2016

American J of Botany

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Our data suggest a genetic basis for pollen donor ability to sire seeds in competition. The significant response to selection in two replicates shows that position of seeds sired can respond to selection. Thus, all components for sexual selection to occur and affect traits are present. Variation in results among replicates might be due to changes in greenhouse conditions. Environmental effects may contribute to the maintenance of variation in these fitness-related characters.

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Effects of virus infection on pollen production and pollen performance: Implications for the spread of resistance alleles

Abstract: ZYMV infection adversely impacts the amount of pollen that can be donated to conspecifics, and pollen competition within the styles increases the probability that the ovules are fertilized by pollen from plants that are thriving when challenged by a viral disease.

Cited by 15 publications

References 49 publications

Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?

Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?

Zucchini Yellow Mosaic Virus Infection Limits Establishment and Severity of Powdery Mildew in Wild Populations of Cucurbita pepo

Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, Raphanus sativus

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