Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split

Self-incompatibility (SI) is found in approximately 40% of flowering plant species and at least 100 families. Although orchids belong to the largest angiosperm family, only 10% of orchid species present SI and have gametophytic SI (GSI). Furthermore, a majority (72%) of Dendrobium species, which con...

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Main Authors: Shan-Ce Niu, Jie Huang, Yong-Qiang Zhang, Pei-Xing Li, Guo-Qiang Zhang, Qing Xu, Li-Jun Chen, Jie-Yu Wang, Yi-Bo Luo, Zhong-Jian Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.01106/full
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author Shan-Ce Niu
Shan-Ce Niu
Shan-Ce Niu
Jie Huang
Yong-Qiang Zhang
Pei-Xing Li
Guo-Qiang Zhang
Qing Xu
Li-Jun Chen
Jie-Yu Wang
Yi-Bo Luo
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
author_facet Shan-Ce Niu
Shan-Ce Niu
Shan-Ce Niu
Jie Huang
Yong-Qiang Zhang
Pei-Xing Li
Guo-Qiang Zhang
Qing Xu
Li-Jun Chen
Jie-Yu Wang
Yi-Bo Luo
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
author_sort Shan-Ce Niu
collection DOAJ
description Self-incompatibility (SI) is found in approximately 40% of flowering plant species and at least 100 families. Although orchids belong to the largest angiosperm family, only 10% of orchid species present SI and have gametophytic SI (GSI). Furthermore, a majority (72%) of Dendrobium species, which constitute one of the largest Orchidaceae genera, show SI and have GSI. However, nothing is known about the molecular mechanism of GSI. The S-determinants of GSI have been well characterized at the molecular level in Solanaceae, Rosaceae, and Plantaginaceae, which use an S-ribonuclease (S-RNase)-based system. Here, we investigate the hypothesis that Orchidaceae uses a similar S-RNase to those described in Rosaceae, Solanaceae, and Plantaginaceae SI species. In this study, two SI species (Dendrobium longicornu and D. chrysanthum) were identified using fluorescence microscopy. Then, the S-RNase- and SLF-interacting SKP1-like1 (SSK1)-like genes present in their transcriptomes and the genomes of Phalaenopsis equestris, D. catenatum, Vanilla shenzhenica, and Apostasia shenzhenica were investigated. Sequence, phylogenetic, and tissue-specific expression analyses revealed that none of the genes identified was an S-determinant, suggesting that Orchidaceae might have a novel SI mechanism. The results also suggested that RNase-based GSI might have evolved after the split of monocotyledons (monocots) and dicotyledons (dicots) but before the split of Asteridae and Rosidae. This is also the first study to investigate S-RNase-based GSI in monocots. However, studies on gene identification, differential expression, and segregation analyses in controlled crosses are needed to further evaluate the genes with high expression levels in GSI tissues.
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spelling doaj.art-669c9e0a1a944379aa0bf81ccdcbb2af2022-12-22T03:21:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-06-01810.3389/fpls.2017.01106254739Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot SplitShan-Ce Niu0Shan-Ce Niu1Shan-Ce Niu2Jie Huang3Yong-Qiang Zhang4Pei-Xing Li5Guo-Qiang Zhang6Qing Xu7Li-Jun Chen8Jie-Yu Wang9Yi-Bo Luo10Zhong-Jian Liu11Zhong-Jian Liu12Zhong-Jian Liu13Zhong-Jian Liu14State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesBeijing, ChinaGraduate University of the Chinese Academy of SciencesBeijing, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesBeijing, ChinaShenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Centre of China and The Orchid Conservation and Research Centre of ShenzhenShenzhen, ChinaThe Centre for Biotechnology and BioMedicine, Graduate School at Shenzhen, Tsinghua UniversityShenzhen, ChinaCollege of Forestry and Landscape Architecture, South China Agricultural UniversityGuangzhou, ChinaCollege of Arts, College of Landscape Architecture, Fujian Agriculture and Forestry UniversityFuzhou, ChinaSelf-incompatibility (SI) is found in approximately 40% of flowering plant species and at least 100 families. Although orchids belong to the largest angiosperm family, only 10% of orchid species present SI and have gametophytic SI (GSI). Furthermore, a majority (72%) of Dendrobium species, which constitute one of the largest Orchidaceae genera, show SI and have GSI. However, nothing is known about the molecular mechanism of GSI. The S-determinants of GSI have been well characterized at the molecular level in Solanaceae, Rosaceae, and Plantaginaceae, which use an S-ribonuclease (S-RNase)-based system. Here, we investigate the hypothesis that Orchidaceae uses a similar S-RNase to those described in Rosaceae, Solanaceae, and Plantaginaceae SI species. In this study, two SI species (Dendrobium longicornu and D. chrysanthum) were identified using fluorescence microscopy. Then, the S-RNase- and SLF-interacting SKP1-like1 (SSK1)-like genes present in their transcriptomes and the genomes of Phalaenopsis equestris, D. catenatum, Vanilla shenzhenica, and Apostasia shenzhenica were investigated. Sequence, phylogenetic, and tissue-specific expression analyses revealed that none of the genes identified was an S-determinant, suggesting that Orchidaceae might have a novel SI mechanism. The results also suggested that RNase-based GSI might have evolved after the split of monocotyledons (monocots) and dicotyledons (dicots) but before the split of Asteridae and Rosidae. This is also the first study to investigate S-RNase-based GSI in monocots. However, studies on gene identification, differential expression, and segregation analyses in controlled crosses are needed to further evaluate the genes with high expression levels in GSI tissues.http://journal.frontiersin.org/article/10.3389/fpls.2017.01106/fullOrchidaceaeself-incompatibilityevolutiontranscriptomics and genomicsS-RNase-based GSI
spellingShingle Shan-Ce Niu
Shan-Ce Niu
Shan-Ce Niu
Jie Huang
Yong-Qiang Zhang
Pei-Xing Li
Guo-Qiang Zhang
Qing Xu
Li-Jun Chen
Jie-Yu Wang
Yi-Bo Luo
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
Zhong-Jian Liu
Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
Frontiers in Plant Science
Orchidaceae
self-incompatibility
evolution
transcriptomics and genomics
S-RNase-based GSI
title Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
title_full Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
title_fullStr Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
title_full_unstemmed Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
title_short Lack of S-RNase-Based Gametophytic Self-Incompatibility in Orchids Suggests That This System Evolved after the Monocot-Eudicot Split
title_sort lack of s rnase based gametophytic self incompatibility in orchids suggests that this system evolved after the monocot eudicot split
topic Orchidaceae
self-incompatibility
evolution
transcriptomics and genomics
S-RNase-based GSI
url http://journal.frontiersin.org/article/10.3389/fpls.2017.01106/full
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