The evolutionary history of plant T2/S-type ribonucleases

Abstract

A growing number of T2/S-RNases are being discovered in plant genomes. Members of this protein family have a variety of known functions, but the vast majority are still uncharacterized. We present data and analyses of phylogenetic relationships among T2/S-RNases, and pay special attention to the group that contains the female component of the most widespread system of self-incompatibility in flowering plants. The returned emphasis on the initially identified component of this mechanism yields important conjectures about its evolutionary context. First, we find that the clade involved in self-rejection (class III) is found exclusively in core eudicots, while the remaining clades contain members from other vascular plants. Second, certain features, such as intron patterns, isoelectric point, and conserved amino acid regions, help differentiate S-RNases, which are necessary for expression of self-incompatibility, from other T2/S-RNase family members. Third, we devise and present a set of approaches to clarify new S-RNase candidates from existing genome assemblies. We use genomic features to identify putative functional and relictual S-loci in genomes of plants with unknown mechanisms of self-incompatibility. The widespread occurrence of possible relicts suggests that the loss of functional self-incompatibility may leave traces long after the fact, and that this manner of molecular fossil-like data could be an important source of information about the history and distribution of both RNase-based and other mechanisms of self-incompatibility. Finally, we release a public resource intended to aid the search for S-locus RNases, and help provide increasingly detailed information about their taxonomic distribution.

Stochastic Character Mapping of State-Dependent Diversification Reveals the Tempo of Evolutionary Decline in Self-Compatible Onagraceae Lineages

“…The system of SI found in Onagraceae is S-RNase-based gametophytic SI (Raven 1979;Franklin et al 1995;Igic et al 2008). This system of SI evolved once in the common ancestor of the Asteridae and Rosidae (Steinbachs and Holsinger 2002;Igic et al 2008;Vieira et al 2008;Niu et al 2017;Ramanauskas and Igić 2017), the clade that contains Onagraceae. Raven (1979) writes the system of SI in Onagraceae "is gametophytic, and involves a series of S-a1leles, with inhibition of pollen-tube growth normally in the surface layers of the stigma."…”

RNase‐based self‐incompatibility in cacti

“…Some unusual features of RSI can, however, be harnessed to overcome the usual obstacles present in uncovering the genetic bases of traits. First, the wide phylogenetic distribution of RSI indicates that T2/S‐RNases are clear pistil‐part expression candidates in eudicots with unknown basis of SI (Ramanauskas & Igić, 2017). A subset of members in this gene family can be identified by a set of unique structural features, as well as their phylogenetic relationships (Igić & Kohn, 2001; Steinbachs & Holsinger, 2002; Vieira et al ., 2008; Ramanauskas & Igić, 2017).…”

Primary restriction of S‐RNase cytotoxicity by a stepwise ubiquitination and degradation pathway in Petuniahybrida

“…T2 RNases are widespread in every organism except Archaea and are involved in a variety of biological processes, including phosphate starvation, viral infection, self‐fertilisation, tumour growth control and cell death (Löffler et al ., 1992; Bariola et al ., 1994; Meyers et al ., 1999; Thompson & Parker, 2009; Ramanauskas & Igić, 2017). However, our understanding of their function remains largely incomplete, especially when their roles appear to be independent of their enzymatic activity.…”