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Ecophysiological and biophysical constraints on domestication in crop plants

Periodic Reporting for period 3 - CONSTRAINTS (Ecophysiological and biophysical constraints on domestication in crop plants)

Reporting period: 2018-06-01 to 2019-11-30

A fundamental question in biology is how constraints drive phenotypic changes and the diversification of life. While domesticated species are extraordinary models for tracking phenotypic changes in response to directional selection, we know little about the role of these constraints on crop domestication, nor how artificial selection can escape them.

Crop yields experienced spectacular growth during the Green Revolution thanks to plant breeding and agronomic development. Yet, crop improvement has not seen comparable advances for increased productivity in the last decades. Artificial selection over preexisting natural variation might have reached a dead end, and the environmental impacts of intensified agronomy are unsustainable in the long term. Thus, plant breeding may have to look for novel strategies to ensure food security and environmental sustainability for a steadily increasing human world population, including the creation of ideotypes adapted to low-input agricultural management. While new biotechnological tools producing ‘super-domesticates’ may offer qualitative advancement in breeding for higher productivity, plant breeding approaches rarely account for ecophysiological and biophysical constraints - linked to resource capture, use and partitioning - that can strongly limit the improvement of the basic functions of plants: growth, reproduction and survival. These constraints arise from trade-offs (i.e. the impossibility to simultaneously optimize two conflicting functions) that take place at different organizational levels: cell, organ, organism and crop (monoculture and mixture). These constraints are considered as obstacles for the improvement of target crop traits by plant breeders but their quantification remains scarce. Interestingly, several generic, cross-species, ecophysiological and biophysical constraints have been identified in theoretical and empirical ecology, with an acceleration in the last two decades with the rising of trait-based ecology. The CONSTRAINTS project aims at examining the persistence of these constraints, found across wild species, within and between domesticated species and the possibility to overcome them in future tradeoff-free improvement approaches. We primarily focus on ecophysiological and biophysical constraints at two organization levels: at the organ level (in particular leaves and roots) and at the whole-plant level. We will investigate other organs (including grains and stems) and other organizational levels: cell and crop.
There are three key milestones that the CONSTRAINTS team has accomplished.
First, the databasing task is pivotal to the CONSTRAINTS project. The PI has participated to major works dedicated to compute a root trait database. He also contributed to the BIEN database that delivers trait data and occurrence data of > 200,000 plant species. The team has made major advancements in the development of the CropTraits database thanks to the work of Justine Bresson hired for this task (in replacement of Marianne Gerard). The structure of the database is completed and > 5,000 data have been entered. A website (http://erc-constraints.cefe.cnrs.fr/database-croptraits/) has been created to facilitate interactions with data providers (mostly the collaborators of the CONSTRAINTS project for now) and to further serve the data. Two workshops have been organized during the reporting period to discuss the structure of the database, the species and type of traits to include.
Second, the development of the ‘functional rarity’ concept is a major achievement of the CONSTRAINTS project. The general idea was to find a method to test whether and how crop species can be considered as functional outlier (or functionally rare species) compared to wild species. This led to a very general concept that can be applied in many contexts. Matthias Grenié and Nicolas Loiseau have been hired to develop this concept (R package, case study, data analyses). Two workshops were organized with French and international collaborators to build on the functional rarity project.
Third, the team spent a major part of its time on the experimental test of allometric relationships, notably using the model species Arabidopsis thaliana. Helena Bestova grew 130 genotypes of A. thaliana in the greenhouse of the host institution. She measured whole-plant photosynthesis and respiration (after having prototyped a specific chamber with artificial light to assess whole-plant C02 exchanges) on these genotypes. Amélie Emmanuel, Helena Bestova and François Vasseur also developed an original protocol to estimate the number of chloroplasts and mitochondria through PCR analyses. The analysis of the allometric relationships between plant biomass, whole-plant photosynthesis, whole-plant respiration, number of chloroplasts and number of mitochondria is very promising. A publication targeted for Nature is in preparation by H. Bestova.
We have rigorously addressed the milestones of his first ERC project and provided the planned deliverables in time. Notably, we have created a crop trait database (CropTraits). This database encompasses plant traits related to resource use (including plant height, specific leaf area, root architecture), measured on isolated plants grown in pots, for 15 crop species and more than 5000 genotypes. We plan to perform a meta-analysis using this complete database with the objective of testing the leaf economics spectrum in crop species.
Calling for Nature-Based Solutions (NBS) in agriculture is a wish widely shared today. At the field level, increasing the cultivated diversity (e.g. by cultivating mixtures of species or mixtures of varieties of a given species – hereafter crop mixtures sensu lato) is often advanced as a NBS to face societal and environmental demands (incl. a demand for reduction of fertilizers and pesticides). One core hypothesis is that species or genotypic interactions could be ‘optimized’ within these crop mixtures. Complementarity among varieties would allow each of them to use resources (e.g. water, phosphorus) differently, thus would minimize negative interactions among them and subsequently maximize crop yield. The reasoning is classic, the validation is less clear. Empirical ecology has rarely been able to experimentally quantify resource-use complementarity among wild species through an ecophysiological perspective because of the myriad of concomitant, sometimes opposing, processes that are at play. We led a pilot experiment using two genotypes of rice (Oryza sativa) from the japonica group. The two genotypes differed only for one modified QTL associated to root depth (isogenic lines). We found that that the use of soil phosphorus can be finely modulated in the bi-genotype mixture compared to the monoculture of each genotype. In other words, even if resource-use complementarity can be difficult to isolate and quantify in natural communities, it could be maximized in ‘artificial’ communities where phenotypes are better characterized and selected in purpose. This is the challenge we proposed for varietal selection in an opinion paper (Litrico & Violle 2015). We have recently set up a larger experiment using 200 wheat genotypes. We expect to generalize the results of the rice experiment with this novel experiment.
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