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Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly

BACKGROUND: The evolution of heterostyly, a genetically controlled floral polymorphism, has been a hotspot of research since the 19th century. In recent years, studies on the molecular mechanism of distyly (the most common form of heterostyly) revealed an evolutionary convergence in genes for brassi...

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Autores principales: Luo, Zhonglai, Zhao, Zhongtao, Xu, Yuanqing, Shi, Miaomiao, Tu, Tieyao, Pei, Nancai, Zhang, Dianxiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10060554/
https://www.ncbi.nlm.nih.gov/pubmed/37008460
http://dx.doi.org/10.3389/fpls.2023.1116078
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author Luo, Zhonglai
Zhao, Zhongtao
Xu, Yuanqing
Shi, Miaomiao
Tu, Tieyao
Pei, Nancai
Zhang, Dianxiang
author_facet Luo, Zhonglai
Zhao, Zhongtao
Xu, Yuanqing
Shi, Miaomiao
Tu, Tieyao
Pei, Nancai
Zhang, Dianxiang
author_sort Luo, Zhonglai
collection PubMed
description BACKGROUND: The evolution of heterostyly, a genetically controlled floral polymorphism, has been a hotspot of research since the 19th century. In recent years, studies on the molecular mechanism of distyly (the most common form of heterostyly) revealed an evolutionary convergence in genes for brassinosteroids (BR) degradation in different angiosperm groups. This floral polymorphism often exhibits considerable variability that some taxa have significant stylar dimorphism, but anther height differs less. This phenomenon has been termed “anomalous” distyly, which is usually regarded as a transitional stage in evolution. Compared to “typical” distyly, the genetic regulation of “anomalous” distyly is almost unknown, leaving a big gap in our understanding of this special floral adaptation strategy. METHODS: Here we performed the first molecular-level study focusing on this floral polymorphism in Guettarda speciosa (Rubiaceae), a tropical tree with “anomalous” distyly. Comprehensive transcriptomic profiling was conducted to examine which genes and metabolic pathways were involved in the genetic control of style dimorphism and if they exhibit similar convergence with “typical” distylous species. RESULTS: “Brassinosteroid homeostasis” and “plant hormone signal transduction” was the most significantly enriched GO term and KEGG pathway in the comparisons between L- and S-morph styles, respectively. Interestingly, homologs of all the reported S-locus genes either showed very similar expressions between L- and S-morph styles or no hits were found in G. speciosa. BKI1, a negative regulator of brassinosteroid signaling directly repressing BRI1 signal transduction, was identified as a potential gene regulating style length, which significantly up-regulated in the styles of S-morph. DISCUSSION: These findings supported the hypothesis that style length in G. speciosa was regulated through a BR-related signaling network in which BKI1 may be one key gene. Our data suggested, in species with “anomalous” distyly, style length was regulated by gene differential expressions, instead of the “hemizygous” S-locus genes in “typical” distylous flowers such as Primula and Gelsemium, representing an “intermediate” stage in the evolution of distyly. Genome-level analysis and functional studies in more species with “typical” and “anomalous” distyly would further decipher this “most complex marriage arrangement” in angiosperms and improve our knowledge of floral evolution.
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spelling pubmed-100605542023-03-31 Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly Luo, Zhonglai Zhao, Zhongtao Xu, Yuanqing Shi, Miaomiao Tu, Tieyao Pei, Nancai Zhang, Dianxiang Front Plant Sci Plant Science BACKGROUND: The evolution of heterostyly, a genetically controlled floral polymorphism, has been a hotspot of research since the 19th century. In recent years, studies on the molecular mechanism of distyly (the most common form of heterostyly) revealed an evolutionary convergence in genes for brassinosteroids (BR) degradation in different angiosperm groups. This floral polymorphism often exhibits considerable variability that some taxa have significant stylar dimorphism, but anther height differs less. This phenomenon has been termed “anomalous” distyly, which is usually regarded as a transitional stage in evolution. Compared to “typical” distyly, the genetic regulation of “anomalous” distyly is almost unknown, leaving a big gap in our understanding of this special floral adaptation strategy. METHODS: Here we performed the first molecular-level study focusing on this floral polymorphism in Guettarda speciosa (Rubiaceae), a tropical tree with “anomalous” distyly. Comprehensive transcriptomic profiling was conducted to examine which genes and metabolic pathways were involved in the genetic control of style dimorphism and if they exhibit similar convergence with “typical” distylous species. RESULTS: “Brassinosteroid homeostasis” and “plant hormone signal transduction” was the most significantly enriched GO term and KEGG pathway in the comparisons between L- and S-morph styles, respectively. Interestingly, homologs of all the reported S-locus genes either showed very similar expressions between L- and S-morph styles or no hits were found in G. speciosa. BKI1, a negative regulator of brassinosteroid signaling directly repressing BRI1 signal transduction, was identified as a potential gene regulating style length, which significantly up-regulated in the styles of S-morph. DISCUSSION: These findings supported the hypothesis that style length in G. speciosa was regulated through a BR-related signaling network in which BKI1 may be one key gene. Our data suggested, in species with “anomalous” distyly, style length was regulated by gene differential expressions, instead of the “hemizygous” S-locus genes in “typical” distylous flowers such as Primula and Gelsemium, representing an “intermediate” stage in the evolution of distyly. Genome-level analysis and functional studies in more species with “typical” and “anomalous” distyly would further decipher this “most complex marriage arrangement” in angiosperms and improve our knowledge of floral evolution. Frontiers Media S.A. 2023-03-16 /pmc/articles/PMC10060554/ /pubmed/37008460 http://dx.doi.org/10.3389/fpls.2023.1116078 Text en Copyright © 2023 Luo, Zhao, Xu, Shi, Tu, Pei and Zhang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Luo, Zhonglai
Zhao, Zhongtao
Xu, Yuanqing
Shi, Miaomiao
Tu, Tieyao
Pei, Nancai
Zhang, Dianxiang
Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title_full Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title_fullStr Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title_full_unstemmed Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title_short Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with “anomalous” distyly
title_sort comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in guettarda speciosa (rubiaceae), a species with “anomalous” distyly
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10060554/
https://www.ncbi.nlm.nih.gov/pubmed/37008460
http://dx.doi.org/10.3389/fpls.2023.1116078
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