Restoring pistil‐side self‐incompatibility factors recapitulates an interspecific reproductive barrier between tomato species

Abstract

SUMMARYInterspecific reproductive barriers are poorly understood, but are central to the biological species concept. The pre-zygotic barriers between red-and green-fruited species in the tomato clade of the genus Solanum provide a model to better understand these barriers in plants. Compatibility usually follows the SI x SC rule: pollen from self-compatible (SC) red-fruited species is rejected on pistils of the predominantly self-incompatible (SI) green-fruited species, but the reciprocal crosses are compatible. This suggests that the interspecific reproductive barrier may be linked to the intraspecific SI mechanism. However, pollen from the SC red-fruited species is also rejected by SC accessions of green-fruited species that lack S-RNase, a key protein expressed in pistils of SI Solanum species. Thus, multiple mechanisms may contribute to the barrier between red-and green-fruited species. We tested whether an S-RNase-dependent barrier is sufficient for rejection of pollen from red-fruited species by introducing functional S-RNase, HT-A and HT-B genes from SI species into Solanum lycopersicum (cultivated tomato). We found that expressing S-RNase in combination with either HT-A or HT-B in the pistil is sufficient to cause rejection of pollen from all four red-fruited species. Thus, redundant mechanisms must operate side by side to prevent crosses between red-and greenfruited species in the clade, underlining the complexity of interspecific pollination barriers. Our results also have implications for mating system transitions. We suggest that these transitions must occur in a specific sequence, and that the transition from SI to SC also affects interspecific compatibility.

Pollen-Pistil Interactions and Their Role in Mate Selection

“…The tomato clade offers additional insights, because its interspecific crossing relationships are better characterized than are Nicotiana's. Expressing S-RNase and HT genes in SC S. lycopersicum, which normally lacks UI barriers, caused the rejection of pollen from all of the redfruited SC tomato species but not from any green-fruited tomato species (Tovar-Méndez et al, 2014). Taken together, these studies clearly demonstrate that pistil-side SI and UI barriers share genetic factors.…”

“…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.…”

“…SI is exquisitely specific and only causes the rejection of pollen with specific S-haplotypes, while UI interspecific pollen rejection causes the rejection of pollen from entire species or clades (Murfett et al, 1996;Beecher et al, 2001;Tovar-Méndez et al, 2014). Lewis and Crowe (1958) noted that pistils with any functional S-locus could inhibit interspecific SC pollen, and they referred to this as unitary action.…”

Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

“…This observation suggested that ui6.1-and by extension, ui1.1-is required for pollen resistance to S-RNase-based rejection in the pistil. Interestingly, neither ui6.1 nor ui1.1 is required for resistance to S-RNase itself, because tomato pollen is fully compatible on pistils expressing active S-RNase in the absence of a functional HT protein (15,22). Thus, both SI and UI require multiple pollen and pistil factors.…”

“…This unidirectional pattern of pollen rejection is referred to as the "SI × SC rule" (12). Although the mechanisms of pollen recognition and rejection by UI are complex (13), several SI factors, including S-RNase, CUL1, and HT, also function in UI (8,14,15).…”