Comparative transcriptomics identifies candidate genes involved in the evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae)

Lydia Gramzow; Katharina Klupsch; Noé Fernández-Pozo; Martin Hölzer; Manja Marz; Stefan A Rensing; Günter Theißen

doi:10.1186/s12870-022-03631-8

Comparative transcriptomics identifies candidate genes involved in the evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae)

BMC Plant Biol. 2022 Jul 14;22(1):340. doi: 10.1186/s12870-022-03631-8.

Authors

Lydia Gramzow¹, Katharina Klupsch¹, Noé Fernández-Pozo^{2

3}, Martin Hölzer^{4

5}, Manja Marz⁴, Stefan A Rensing^{2

6}, Günter Theißen⁷

Affiliations

¹ Matthias Schleiden Institute / Genetics, Friedrich Schiller University Jena, 07743, Jena, Germany.
² Plant Cell Biology, Department of Biology, University of Marburg, 35043, Marburg, Germany.
³ Departamento de Fruticultura Subtropical y Mediterránea, IHSM - CSIC - UMA, Málaga, 29010, Spain.
⁴ RNA Bioinformatics and High-Throughput Analysis, Friedrich Schiller University Jena, 07743, Jena, Germany.
⁵ Present Address: Methodology and Research Infrastructure/Bioinformatics, Robert Koch Institute, 13353, Berlin, Germany.
⁶ Centre for Biological Signaling Studies (BIOSS), University of Freiburg, 79108, Freiburg, Germany.
⁷ Matthias Schleiden Institute / Genetics, Friedrich Schiller University Jena, 07743, Jena, Germany. guenter.theissen@uni-jena.de.

Abstract

Background: Fruits are the seed-bearing structures of flowering plants and are highly diverse in terms of morphology, texture and maturation. Dehiscent fruits split open upon maturation to discharge their seeds while indehiscent fruits are dispersed as a whole. Indehiscent fruits evolved from dehiscent fruits several times independently in the crucifer family (Brassicaceae). The fruits of Lepidium appelianum, for example, are indehiscent while the fruits of the closely related L. campestre are dehiscent. Here, we investigate the molecular and genetic mechanisms underlying the evolutionary transition from dehiscent to indehiscent fruits using these two Lepidium species as model system.

Results: We have sequenced the transcriptomes and small RNAs of floral buds, flowers and fruits of L. appelianum and L. campestre and analyzed differentially expressed genes (DEGs) and differently differentially expressed genes (DDEGs). DEGs are genes that show significantly different transcript levels in the same structures (buds, flowers and fruits) in different species, or in different structures in the same species. DDEGs are genes for which the change in expression level between two structures is significantly different in one species than in the other. Comparing the two species, the highest number of DEGs was found in flowers, followed by fruits and floral buds while the highest number of DDEGs was found in fruits versus flowers followed by flowers versus floral buds. Several gene ontology terms related to cell wall synthesis and degradation were overrepresented in different sets of DEGs highlighting the importance of these processes for fruit opening. Furthermore, the fruit valve identity genes FRUITFULL and YABBY3 were among the DEGs identified. Finally, the microRNA miR166 as well as the TCP transcription factors BRANCHED1 (BRC1) and TCP FAMILY TRANSCRIPTION FACTOR 4 (TCP4) were found to be DDEGs.

Conclusions: Our study reveals differences in gene expression between dehiscent and indehiscent fruits and uncovers miR166, BRC1 and TCP4 as candidate genes for the evolutionary transition from dehiscent to indehiscent fruits in Lepidium.

Keywords: Dehiscence; Differentially expressed genes; Fruit development; Lepidium appelianum; Lepidium campestre; Transcriptome.

MeSH terms

Brassicaceae* / genetics
Brassicaceae* / metabolism
Flowers / genetics
Fruit / genetics
Fruit / metabolism
Gene Expression Regulation, Plant
Lepidium* / genetics
Transcriptome