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Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species.
Plant J 2014; 77(5):727-36PJ

Abstract

Interspecific 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 green-fruited 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.

Authors+Show Affiliations

Division of Biochemistry, University of Missouri-Columbia, 117 Schweitzer Hall, Columbia, MO, 65211, USA.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

24387692

Citation

Tovar-Méndez, Alejandro, et al. "Restoring Pistil-side Self-incompatibility Factors Recapitulates an Interspecific Reproductive Barrier Between Tomato Species." The Plant Journal : for Cell and Molecular Biology, vol. 77, no. 5, 2014, pp. 727-36.
Tovar-Méndez A, Kumar A, Kondo K, et al. Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species. Plant J. 2014;77(5):727-36.
Tovar-Méndez, A., Kumar, A., Kondo, K., Ashford, A., Baek, Y. S., Welch, L., ... McClure, B. A. (2014). Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species. The Plant Journal : for Cell and Molecular Biology, 77(5), pp. 727-36. doi:10.1111/tpj.12424.
Tovar-Méndez A, et al. Restoring Pistil-side Self-incompatibility Factors Recapitulates an Interspecific Reproductive Barrier Between Tomato Species. Plant J. 2014;77(5):727-36. PubMed PMID: 24387692.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Restoring pistil-side self-incompatibility factors recapitulates an interspecific reproductive barrier between tomato species. AU - Tovar-Méndez,Alejandro, AU - Kumar,Aruna, AU - Kondo,Katsuhiko, AU - Ashford,Amy, AU - Baek,You S, AU - Welch,Lillian, AU - Bedinger,Patricia A, AU - McClure,Bruce A, Y1 - 2014/02/11/ PY - 2013/10/14/received PY - 2013/12/16/revised PY - 2013/12/18/accepted PY - 2014/1/7/entrez PY - 2014/1/7/pubmed PY - 2015/3/31/medline KW - Solanum KW - gametophytic self-incompatibility KW - interspecific compatibility KW - mating system KW - tomato KW - unilateral incompatibility SP - 727 EP - 36 JF - The Plant journal : for cell and molecular biology JO - Plant J. VL - 77 IS - 5 N2 - Interspecific 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 green-fruited 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. SN - 1365-313X UR - https://www.unboundmedicine.com/medline/citation/24387692/Restoring_pistil_side_self_incompatibility_factors_recapitulates_an_interspecific_reproductive_barrier_between_tomato_species_ L2 - https://doi.org/10.1111/tpj.12424 DB - PRIME DP - Unbound Medicine ER -