Mating system transitions in Solanum habrochaites impact interactions between populations and species

Abstract

SummaryIn plants, transitions in mating system from outcrossing to self-fertilization are common; however, the impact of these transitions on interspecific and interpopulation reproductive barriers is not fully understood. We examined the consequences of mating system transition for reproductive barriers in 19 populations of the wild tomato species Solanum habrochaites.We identified S. habrochaites populations with self-incompatible (SI), self-compatible (SC) and mixed population (MP) mating systems, and characterized pollen-pistil interactions among S. habrochaites populations and between S. habrochaites and other tomato species. We examined the relationship between mating system, floral morphology, interspecific and interpopulation compatibility and pistil SI factors.We documented five distinct phenotypic groups by combining reproductive behavior with molecular data. Transitions from SI to MP were not associated with weakened interspecific reproductive barriers or loss of known pistil SI factors. However, transitions to SC at the northern range margin were accompanied by loss of S-RNase, smaller flowers, and weakened (or absent) interspecific pollenÀpistil barriers. Finally, we identified a subset of SC populations that exhibited a partial interpopulation reproductive barrier with central SI populations.Our results support the hypothesis that shifts in mating system, followed by additional lossof-function mutations, impact reproductive barriers within and between species.

Pollen-Pistil Interactions and Their Role in Mate Selection

“…Redundancy is apparent in systems where gain-of-function studies show that pollen that is susceptible to S-RNase-dependent rejection (such as the Nicotiana and tomato studies described earlier; Murfett et al, 1996;Beecher et al, 2001;Tovar-Méndez et al, 2014) can also be rejected by SC accessions that entirely lack S-RNase (Martin, 1961;Murfett et al, 1996;Covey et al, 2010;Chalivendra et al, 2013;Tovar-Méndez et al, 2014;Baek et al, 2015;Broz et al, 2017). Redundancy complicates analysis, but the mechanisms can be elucidated through a combination of gain-and loss-of-function studies.…”

HT proteins contribute to S‐RNase‐independent pollen rejection in Solanum

“…Still, we do not conclude that the corresponding SI progenitors necessarily express only this barrier and the S-RNase-independent/HTdependent mechanism. For example, SC S. habrochaites LA0407 is a more derived SC accession (i.e., compared to other SC accessions) collected about 200 km north of the nearest SI population of S. habrochaites, and it appears to have undergone several additional changes after loss of SI (Broz et al, 2016).…”

“…However, S. habrochaites is exceptional, as only HT-A is functional in this species (Covey et al, 2010). Broz et al (2016) recently described an accession from the extreme northern part of the S. habrochaites range -SC S. habrochaites LA1223that has mutations in S-RNase, HT-A, and HT-B genes. As expected, this accession accepts pollen from S. lycopersicum and other tomato clade species (Broz et al, 2016) due to the progressive loss of redundant pollen rejection mechanisms.…”

Linking gene expression to unilateral pollen-pistil reproductive barriers

“…In a number of plant families, including the Solanaceae, a 28 unidirectional post-mating prezygotic barrier termed unilateral incompatibility (UI) occurs at the 29 level of pollen-pistil interactions. UI has most often been studied between genera or species [1-30 5], but there is also evidence of UI between populations of the same species [1,[6][7][8][9].…”

“…A number of studies have examined both the physiological aspects [1,5,42,43] and 64 5 genetic basis [26-28, 30, 31, 33] of UI between members of the clade. In addition, a small 65 number of studies have assessed UI between SI and SC populations within a species [1,[6][7][8][9]43]. 66 The wild tomato Solanum habrochaites is an ideal species in which to study both 67 interspecific and interpopulation UI within the context of recently diverged populations.…”