Roles of the APETALA3-3 ortholog in the petal identity specification and morphological differentiation in Delphinium anthriscifolium flowers

Abstract

The genus Delphinium (Ranunculaceae) with its unique and highly complex floral structure is an ideal system to address some key questions in terms of morphological and evolutionary studies in flowers. In D. anthriscifolium, for example, the original eight petal primordia differentiate into three types at maturity (i.e., two dorsal spurred, two lateral flat, and four ventral reduced petals). The mechanisms underlying their identity determination and morphological differentiation remain unclear. Here, through a comprehensive approach combining digital gene expression (DGE) profiles, in situ hybridization, and virus-induced gene silencing (VIGS), we explore the role of the APETALLATA3-3 (AP3-3) ortholog in D. anthriscifolium. Our findings reveal that the DeanAP3-3 not only functions as a traditionally known petal identity gene but also plays a critical role in petal morphological differentiation. The DeanAP3-3 gene is expressed in all the petal primordia before their morphological differentiation at earlier stages, but shows a gradient expression level difference along the dorsventral floral axis, with higher expression level in the dorsal spurred petals, intermediate level in the lateral flat petals and lower level in the ventral reduced petals. VIGS experiments revealed that flowers with strong phenotypic changes showed a complete transformation of all the three types of petals into non-spurred sepals. However, in the flowers with moderate phenotypic changes, the transformation of spurred petals into flat petals is associated with moderate silencing of the DeanAP3-3 gene, suggesting a significant impact of expression level on petal morphological differentiation. This research also shed some insights into the role of changes in gene expression levels on morphological differentiation in plants.

Acknowledgements

We would like to thank Dr. Hongzhi Kong and Hongyan Shan for valuable comments and suggestions, and the editors and the two anonymous reviewers for their insightful suggestions. Some texts in this paper were polished by Stork’s Writing Assistant (https://www.storkapp.me/writeassistant/). This work was supported by National Natural Science Foundation of China grant (32372750 and 31970247), Qin Chuangyuan High-level Innovation and Entrepreneur-ship Talent Program (2021QCYRC4-51), and the Fundamental Research Funds for Northwest A&F University.

Author contributions

R.Z., L.G., and P.Z. conceived and designed the experiments. P.Z., Y.X., W.X., L.L., H.Z., and R.Z. collected the plant samples. P.Z., H.Z., Y.X., L.L., and W.X. performed the experiment. P.Z. and L.G. analysed the data and performed the visualization. L.G., R.Z., and P.Z. contributed to the writing and revision of the manuscript. All authors read and approved the final paper.

Data availability

All data supporting the conclusions of this study may be found in the publication and its supplemental materials, which are available online. Any additional relevant information can be obtained from the corresponding authors upon request (Liping Guo and Rui Zhang).

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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