Comparative Evidence for the Correlated Evolution of Polyploidy and Self-Compatibility in Solanaceae

Abstract

Breakdown of self-incompatibility occurs repeatedly in flowering plants with important evolutionary consequences. In plant families in which self-incompatibility is mediated by S-RNases, previous evidence suggests that polyploidy may often directly causeself-compatibility through the formation of diploid pollen grains. We use three approaches to examine relationships between selfincompatibility and ploidy. First, we test whether evolution of self-compatibility and polyploidy is correlated in the nightshade family (Solanaceae), and find the expected close association between polyploidy and self-compatibility. Second, we compare the rate of breakdown of self-incompatibility in the absence of polyploidy against the rate of breakdown that arises as a byproduct of polyploidization, and we find the former to be greater. Third, we apply a novel extension to these methods to show that the relative magnitudes of the macroevolutionary pathways leading to self-compatible polyploids are time dependent. Over small time intervals, the direct pathway from self-incompatible diploids is dominant, whereas the pathway through self-compatible diploids prevails over longer time scales. This pathway analysis is broadly applicable to models of character evolution in which sequential combinations of rates are compared. Finally, given the strong evidence for both irreversibility of the loss of self-incompatibility in the family and the significant association between self-compatibility and polyploidy, we argue that ancient polyploidy is highly unlikely to have occurred within the Solanaceae, contrary to previous claims based on genomic analyses. K E Y W O R D S :Angiosperms, breeding systems, comparative methods, polyploidy, self-incompatibility, statistical phylogenetics.Self-incompatibility (SI) is the common ability of hermaphrodite plants to recognize and reject their own pollen with a genetically based mechanism. Approximately one-half of all extant angiosperm species prevent self-fertilization by deploying SI (Brewbaker 1959;. Although many different mechanisms of SI evolved in flowering plants, a particular system, which uses RNases in the female component of self-rejection, appears to be ancient. It likely originated at least 90 million years ago (mya), and it may cause SI in dozens of extant eudicot families, including some of the most diverse . A notable property of SI systems is the high rate at which they transition to self-compatibility (SC), considered one of the most common evolutionary transitions in plants (Stebbins 1974). Consequently, many individuals, populations, and species do not express SI. Empirical data on the mechanisms that underlie losses of SI are sparse. Although the genetic causes of transitions from SI to SC vary widely (Stone 2002), a significant proportion of such transitions may involve polyploidization (Livermore and

Assessment of genetic diversity and population structure of Tunisian populations of Brachypodium hybridum by SSR markers

“…Polyploidy is considered an important mode of evolution in higher plants (Robertson et al,2011;Sampson and Byrne, 2011). Over the years, this phenomenon has been the focus ofsubstantial and diverse research.…”

Recent Loss of Self-Incompatibility by Degradation of the Male Component in Allotetraploid Arabidopsis kamchatica

“…Whereas polyploidization is known to disrupt SI almost invariably in gametophytic SI systems where specificities are determined by haploid genotypes of gametes [97], [98], in sporophytic SI systems where specificities are determined sporophytically by the diploid parental genotypes, polyploidization in itself does not necessarily induce the loss of SI (e.g., [57]). We speculate that, in sporophytic SI systems such as those of the Brassicaceae, dominance interactions among S -haplogroups might have played an important role in the loss of SI in polyploid species, as is also implied in a study of synthetic interspecific hybrids by Nasrallah et al [99].…”

A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree

“…What is lacking, however, is a robust phylogenetic framework that encompasses species and generic diversity across the family in order to maximise the potential of these new data sources in a wider evolutionary context. Although several studies have focused on understanding evolution of particular characteristics in Solanaceae in a phylogenetic context, including analyses of genome and chromosome evolution [4-6], life history and polyploidy [7-9], floral and fruit morphology [10,11], gene family evolution and sub-functionalization [12-15], and broad-scale biogeographic patterns [16], only a single study has examined character evolution through time [8]. A central problem has been the lack of a robust, densely sampled, dated molecular phylogeny for the entire family.…”