Fungal Symbionts as Manipulators of Plant Reproductive Biology

Abstract

Dryad data: http://dx.doi.org/10.5061/dryad.84c26.abstract: Symbioses have shaped the evolution of life, most notably through the fixation of heritable symbionts into organelles. The inheritance of symbionts promotes mutualism and fixation by coupling partner fitness. However, conflicts arise if symbionts are transmitted through only one sex and can shift host resources toward the sex through which they propagate. Such reproductive manipulators have been documented in animals with separate sexes but not in other phyla or sexual systems. Here we investigated whether the investment in male relative to female reproduction differed between hermaphroditic host plants with versus without a maternally inherited fungal symbiont. Plants with the fungus produced more seeds and less pollen than plants lacking the fungus, resulting in an ∼40% shift in functional gender and a switch from male-biased to female-biased sex allocation. Given the ubiquity of endophytes in plants, reproductive manipulators of hermaphrodites may be widespread in nature.

Reproductive Parasitism: Maternally Inherited Symbionts in a Biparental World

“…Although fungal endophytes are commonly considered defensive mutualists, Gorischek et al (2013) observed that hermaphrodites infected with fungal symbionts had female-biased sex allocation; this is in contrast to the male-biased allocation pattern observed in non-endophyte-infected conspecific individuals obtained through segregation (imperfect maternal inheritance). They also showed greater vegetative propagation, again permitting symbiont maintenance.…”

“…"Reproductive parasitic" behaviors in plants are commonly associated with mutations in the mitochondrial genome, but have recently also been ascribed to heritable fungi (Gorischek et al 2013). Reproductive parasitism in animals is associated with a wide variety of microbial symbionts: viruses, bacteria, unicellular eukaryotes, and fungi that pass from a female to her progeny either inside eggs or through smearing on the outside of eggs followed by trophic acquisition (Terry et al 2004;Nakanishi et al 2008;Duron and Hurst 2013;Gorischek et al 2013). Although many heritable microbes are simply "beneficial symbionts," reproductive parasitism of the type described above is widespread (and may be combined with beneficial impacts on the female host).…”

Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi

“…They provide numerous benefits to plants, including deterring herbivory by producing toxic secondary metabolites (Clay, 1988) and enhancing drought tolerance (Kane, 2011) and nutrient uptake (Malinowski, Alloush, & Belesky, 2000). These effects have important consequences for host plants and their communities; for example, they can bias sex allocation (Gorischek et al, 2013), facilitate host range expansion (Afkhami, McIntyre, & Strauss, 2014), suppress forest succession (Rudgers et al, 2007), negate productivity-diversity relationships (Rudgers, Koslow, & Clay, 2004), and alter plant, herbivore, predator, and decomposer community compositions (Lemons, Clay, & Rudgers, 2005;Finkes et al, 2006;Afkhami & Strauss, 2016).…”

Nonsystemic fungal endophytes increase survival but reduce tolerance to simulated herbivory in subarcticFestuca rubra

“…, Faeth , , Gorischek et al. ). In contrast, studies of nonsystemic fungal symbionts, although fewer in number, show potentially important but highly variable effects on plant fitness and thus their ecological significance is less well understood (Rodriguez et al.…”