H2020 RiceStyle Project: Carpel Evolution: A Walk on the Rice Side

With approximately 352,000 living species on Earth, flowering plants, or angiosperms, constitute the largest and most diverse extant group in the plant kingdom, accounting for approximately 90% of land plant species. The rapid emergence and diversification of angiosperms, documented by fossils, was defined as an "abominable mystery" by Charles Darwin. Undoubtedly, the evolution of new reproductive structures, such as the flower and its female part, the pistil, played a fundamental role in the extraordinary evolutionary success of angiosperms.

However, how these structures evolved, including at the molecular level, remains unknown. Furthermore, after pollination, the pistil and the ovule(s) within it develop into the fruit and seed(s), respectively, which are the edible part of most crops. Therefore, molecular studies of pistil development can help shed light on one of the greatest "secrets" of plant evolution and provide important advantages and tools for targeted crop improvement.

While information on the genetic control of pistil identity and patterning is already available, these data primarily concern Arabidopsis and a few other eudicot model plants. Therefore, these genetic mechanisms could explain pistil evolution in the earliest ancestors of all flowering plants or represent more recent developments reflecting eudicot adaptation. Comparative studies are therefore needed in the other largest and most evolved group of flowering plants, the monocots, and also in basal angiosperms.

This Marie Curie "Ricestyle" initiative aims to clarify part of the "abominable mystery" by comparatively studying pistil development and its genetic basis in rice, which is by far the leading monocot model plant and, along with other cereals, the main source of calories in the human diet. During the first phase of the project, in the laboratory of Prof. Dabing Zhang (Shanghai Jiao Tong University, China), we developed all the necessary tools for the functional characterization of candidate genes that could be involved in the identity and patterning of pistil tissue.

Based on homology with known genes in Arabidopsis thaliana and other eudicot model plants, we searched the rice genome for phylogenetically related and functionally equivalent genes. Our work has resulted in a comprehensive study of the evolutionary history of these gene families, which will inform our functional studies. Furthermore, the collaboration between the two host laboratories enabled the characterization of three additional transcription factors belonging to the SEPALLATA MADS-box subfamily.

These factors confer the identity of all floral organs, including the pistil, and are therefore key regulators that act also upstream in the molecular network for carpel development. The work has been recently published in Plant Physiology (Wu D, Liang W, Zhu W, Chen M, Ferrandiz C, Burton RA, Dreni L, Zhang D. Plant Physiol. December 7, 2017. pii: pp.00704.2017. doi: 10.1104/pp.17.00704). Furthermore, we have isolated a gene encoding a glutaredoxin, important for pistil development in rice. Loss-of-function mutants fail to produce pistils in approximately half of the spikelet; otherwise, they produce reduced pistils.

These results are somewhat unexpected and could represent an evolutionary innovation in monocots or, alternatively, be equally important in dicots, although these remain to be explored. Therefore, they could provide a two-way pathway to improve our understanding of pistil morphogenesis in angiosperms. A first article describing the function of this glutaredoxin and its genetic interaction with floral and carpel identity genes will be forthcoming. In the second phase of the project, we continued phenotyping and characterizing the aforementioned mutants and also created higher-order mutants. Data from these experiments indicated several genes with essential roles in determining correct carpel morphology in rice. We are further characterizing the molecular networks regulated by these genes and aim to publish our findings soon.