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H2020

RiceStyle Report Summary

Project ID: 661678
Funded under: H2020-EU.1.3.2.

Periodic Reporting for period 1 - RiceStyle (Carpel evolution: a walk in the rice side)

Reporting period: 2016-01-01 to 2017-12-31

Summary of the context and overall objectives of the project

Flowering plants (angiosperms) protect their female reproductive structure, the ovule, within a carpel. After the embryo sac is fertilized by the pollen tube, the ovule gradually turns into a seed, and the carpel becomes a fruit. The carpel is thus an evolutionary conserved structure, but showing an outstanding variability in shapes and function. Several transcription factors directing the main aspects of carpel formation and morphogenesis, are quite well characterized in the model eudicot plant Arabidopsis thaliana. More recent evo-devo studies suggest that some of these transcription factors are functionally conserved, at least in eudicot plants. However, this knowledge is far to be complete, especially if we consider the basal angiosperm taxa and monocots. This proposal aims to investigate more in depth these phenomena, using as main model species rice (Oryza sativa), and subsequently to do comparative studies in other evolutionary significant species. The final goal is to achieve a broader knowledge about the transcriptional machinery ruling carpel development, and its degree of functional conservation among the most relevant angiosperm taxa, by means of innovative techniques. The proposal will also allow us to address new evidence about the molecular pathways acting downstream this transcriptional network. The proposal will have a significant impact in basic and future applied research, addressing the Horizon 2020 objective to invest in future jobs and strengthen EU position in research, innovation and technology, sustainable development climate change and excellent science.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

With approximately 352,000 living species on Earth (The Plant List 2013), the flowering plants or angiosperms constitute the largest and most diverse extant group of the plant kingdom, and about 90% of land plant species. The rapid appearance and diversification of angiosperms which is documented by fossils have been defined as ‘abominable mystery’ by Charles Darwin. Certainly, the evolution of new reproductive structures like the flower and its female part, the pistil, had a major role in the extraordinary evolutive success of angiosperms. How these structures evolved, also at molecular level, is however still unknown. In addition, after pollination the pistil and the ovule(s) within develop into fruit and seed(s) respectively, which are the edible part of most crops. Therefore, molecular studies on pistil development can both help clarify one of the bigger ‘secrets’ of plant evolution, and bring significant advantages and tools for targeted crop improvement. Despite information about genetic control of pistil identity and patterning is already available, these data mainly pertain to Arabidopsis and few other eudicot model plants. Therefore, these genetic mechanisms could either explain the evolution of the pistil in the earliest ancestors of all flowering plants, or represent more recent novelties reflecting the adaptation of eudicots. Therefore, comparative studies are needed in the other largest and most evolved group of flowering plants, the monocots, and also in basal angiosperms. This Marie Curie action ‘Ricestyle’ aims to clarify part of the ‘abominable mystery’ by the comparative study of pistil development and its genetic basis in rice, which is by far the main monocot model plant and, together the other cereals, the main source of calories for human diet.

During the first phase of the project, in the Host Laboratory of Prof. Dabing Zhang (Shanghai Jiao Tong University, China) we have developed the mutant and transgenic lines necessary for the functional characterization of the candidate genes which might be involved in pistil tissue identity and patterning. Based on the homology with genes known in Arabidopsis thaliana and other eudicot model plants, we have search in the rice genome for phylogenetically related and functionally equivalent genes. Our work has yielded a complete study of the evolutionary history of these gene families that will be the base for our functional studies. These have been started by obtaining mutants in many of these genes, either by searching available T-DNA collections of initiating CRISPR-Cas9 mediated mutant generation.

In addition, the collaboration between the two Host Labs allowed the characterization of three other transcription factors belonging to the SEPALLATA MADS-box subfamily. These factors act in the formation of all the MADS-box complexes conferring the identity of all the floral organs including the pistil, thus they are master regulators acting upstream DL, NGA, HEC and SPT. The work has been published recently on Plant Physiology (Wu D, Liang W, Zhu W, Chen M, Ferrandiz C, Burton RA, Dreni L, Zhang D. Plant Physiol. 2017 Dec 7. pii: pp.00704.2017. doi: 10.1104/pp.17.00704. [Epub ahead of print]).
Moreover, we have isolated a gene encoding for a glutaredoxin which is important for the pistil development in rice. Loss of function mutants produce pistils with a narrow filiform ovary not containing an ovule and/or missing one stigma. Those pistils that can develop completely have however a normal rate of fertility. These results are somehow unexpected and may represent a monocot evolutionary innovation or, otherwise, be also important in dicots, only unexplored so far. Thus,they may provide a two-way pathway to improve our knowledge in pistil morphogenesis in angiosperms. A first paper describing the function of this glutaredoxin will be submitted soon to Molecular Plant.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

SInce most of the work is in progress, the major conclusions and advances are expected towards the end of the second phase. However, we can say that progress beyond of the art is significant, mainly around the undescribed role of some key developmental genes in rice, such as DL, in carpel development, one of our hypothesis. In addition, the work on SEP genes and glutarredoxin has uncovered new interactions and opened new ideas to incorporate in our model of pistil development.

In this second phase, we plan to complete most of the work plan, and incorporate the results in a new model for pistil development in monocots that until now has been poorly addressed. 2-3 more publications in high impact journals are expected. Understanding how pistils and therefore grains form and develop in monocots may help to increase yield in cereal crops.

The impact on the fellow's career has been significant in this outgoing phase. It has already produced one publication and other in preparation, it has provided a extensive and solid network of collaborations in Asia and Australia, with access to resources of importance, and it has endowed him with an array of leadership abilities. All these has allowed the fellow to apply for a tenure-track position in Spain (programa Ramon y Cajal), now under evaluation.

For the returning phase, impacts are expected to be significant. The main contribution to the host lab and the institute will be implementing research in rice developmental genetics, a long sougth goal of the group. Since Valencia is a rice-growing region, socio-economic implications might be important also in the development of new links to growers and breeders of local varieties.

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