Abstract
Tomato clade species (Solanum sect. Lycopersicon) display multiple interspecific reproductive barriers (IRBs). Some IRBs conform to the SI x SC rule, which describes unilateral incompatibility (UI) where pollen from SC species is rejected on SI species’ pistils, but reciprocal pollinations are successful. However, SC x SC UI also exists, offering opportunities to identify factors that contribute to S-RNase-independent IRBs. For instance, SC Solanum pennellii LA0716 pistils only permit SC Solanum lycopersicum pollen tubes to penetrate to the top third of the pistil, while S. pennellii pollen penetrates to S. lycopersicum ovaries. We identified candidate S. pennellii LA0716 pistil barrier genes based on expression profiles and published results. CRISPR/Cas9 mutants were created in eight candidate genes, and mutants were assessed for changes in S. lycopersicum pollen tube growth. Mutants in a gene designated Defective in Induced Resistance 1-like (SpDIR1L), which encodes a small cysteine-rich protein, permitted S. lycopersicum pollen tubes to grow to the bottom third of the style. We show that SpDIR1L protein accumulation correlates with IRB strength and that species with weak or no IRBs toward S. lycopersicum pollen share a 150 bp deletion in the upstream region of SpDIR1L. These results suggest that SpDIR1L contributes to an S-RNase-independent IRB.
Highlights
Interspecific reproductive barriers (IRBs) are both biologically and practically significant
The prevalence of IRBs that conform to the SI x SC rule implies a relationship with SI because it is the SI pistil that rejects pollen, while the SC species pistil accepts
We refer to this as a barrier/resistance architecture [8,9,10]. This term may describe either SI or IRBs, and the intraspecific S-RNase-based SI system is, the best understood example wherein S-RNase and other factors comprise a pistil barrier and S-locus F-box (SLF) and other factors provide for pollen resistance [8,9,47]
Summary
Interspecific reproductive barriers (IRBs) are both biologically and practically significant. SI species in Solanaceae display S-RNase-based gametophytic SI [7] characterized by pistilexpressed S-RNases and multiple pollen-expressed F-box protein genes encoded at the. The prevalence of IRBs that conform to the SI x SC rule implies a relationship with SI because it is the SI pistil that rejects pollen, while the SC species pistil accepts Experiments confirm this for crosses between red/orange-fruited SC species and green-fruited SI tomato clade species. S-RNase-independent IRBs. For instance, S. lycopersicum (tomato) displays UI with SC accessions of the predominantly SI species S. arcanum, S. habrochaites, and S. pennellii that fail to express active S-RNase [24,29,30,31]. Defective in Induced Resistance 1-like, SpDIR1L, converted the ‘early’ S. lycopersicum pollen rejection phenotype characteristic of S. pennellii. We conclude that SpDIR1L is implicated in an S-RNase-independent IRB between SC S. lycopersicum pollen by SC S. pennellii LA0716
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