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

Zhonglai Luo; Zhongtao Zhao; Yuanqing Xu; Miaomiao Shi; Tieyao Tu; Nancai Pei; Dianxiang Zhang

doi:10.3389/fpls.2023.1116078

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

Front Plant Sci. 2023 Mar 16:14:1116078. doi: 10.3389/fpls.2023.1116078. eCollection 2023.

Authors

Zhonglai Luo^{1

2}, Zhongtao Zhao², Yuanqing Xu³, Miaomiao Shi², Tieyao Tu², Nancai Pei⁴, Dianxiang Zhang²

Affiliations

¹ School of Life Sciences and Medicine, Shandong University of Technology, Zibo, China.
² Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China.
³ Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan, China.
⁴ Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou, China.

Abstract

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.

Keywords: Guettarda speciosa; brassinosteroid signaling; genetic convergence; heterostyly; molecular regulation; “anomalous” distyly.

Grants and funding

This research was supported by the National Natural Science Foundation of China (Grant Nos. 31970252, 31370269, 31970206, 31000109, 31600185), Science and Technology Program of Guangzhou (Grant No. 202002030437), the Science and Technology BasicWork of the Ministry of Science and Technology of China (Grant No. 2013FY111200), the Initial Funding for Doctoral Research from Shandong University of Technology (Grant No. 4041/422047), and scholarship from the China Scholarship Council (Grant No. 201904910155).