Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species.

The arbuscular mycorrhizal (AM) symbiosis is key to plant nutrition, and hence is potentially key in sustainable agriculture. Fertilization and other agricultural practices reduce soil AM fungi and root colonization. Such conditions might promote the evolution of low mycorrhizal responsive crops. Therefore, we ask if and how evolution under domestication has altered AM symbioses of crops. We measured the effect of domestication on mycorrhizal responsiveness across 27 crop species and their wild progenitors. Additionally, in a subset of 14 crops, we tested if domestication effects differed under contrasting phosphorus (P) availabilities. The response of AM symbiosis to domestication varied with P availability. On average, wild progenitors benefited from the AM symbiosis irrespective of P availability, while domesticated crops only profited under P-limited conditions. Magnitudes and directions of response were diverse among the 27 crops, and were unrelated to phylogenetic affinities or to the coordinated evolution with fine root traits. Our results indicate disruptions in the efficiency of the AM symbiosis linked to domestication. Under high fertilization, domestication could have altered the regulation of resource trafficking between AM fungi and associated plant hosts. Provided that crops are commonly raised under high fertilization, this result has important implications for sustainable agriculture.

Side-effects of domestication: cultivated legume seeds contain similar tocopherols and fatty acids but less carotenoids than their wild counterparts.

BACKGROUND: Lipophilic antioxidants play dual key roles in edible seeds (i) as preservatives of cell integrity and seed viability by preventing the oxidation of fats, and (ii) as essential nutrients for human and animal life stock. It has been well documented that plant domestication and post-domestication evolution frequently resulted in increased seed size and palatability, and reduced seed dormancy. Nevertheless, and surprisingly, it is poorly understood how agricultural selection and cultivation affected the physiological fitness and the nutritional quality of seeds. Fabaceae have the greatest number of crop species of all plant families, and most of them are cultivated for their highly nutritious edible seeds. Here, we evaluate whether evolution of plants under cultivation has altered the integrated system formed by membranes (fatty acids) and lipophilic antioxidants (carotenoids and tocopherols), in the ten most economically important grain legumes and their closest wild relatives, i.e.: Arachis (peanut), Cicer (chickpea), Glycine (soybean), Lathyrus(vetch), Lens (lentil), Lupinus (lupin), Phaseolus (bean), Pisum (pea), Vicia (faba bean) and Vigna (cowpea). RESULTS: Unexpectedly, we found that following domestication, the contents of carotenoids, including lutein and zeaxanthin, decreased in all ten species (total carotenoid content decreased 48% in average). Furthermore, the composition of carotenoids changed, whereby some carotenoids were lost in most of the crops. An undirected change in the contents of tocopherols and fatty acids was found, with contents increasing in some species and decreasing in others, independently of the changes in carotenoids. In some species, polyunsaturated fatty acids (linolenic acid especially), α-tocopherol and γ-tocopherol decreased following domestication. CONCLUSIONS: The changes in carotenoids, tocopherols and fatty acids are likely side-effects of the selection for other desired traits such as the loss of seed dormancy and dispersal mechanisms, and selection for seed storability and taste. This work may serve as baseline to broaden our knowledge on the integrated changes on crop fitness and nutritional quality following domestication.

Shifts and disruptions in resource-use trait syndromes during the evolution of herbaceous crops.

Trait-based ecology predicts that evolution in high-resource agricultural environments should select for suites of traits that enable fast resource acquisition and rapid canopy closure. However, crop breeding targets specific agronomic attributes rather than broad trait syndromes. Breeding for specific traits, together with evolution in high-resource environments, might lead to reduced phenotypic integration, according to predictions from the ecological literature. We provide the first comprehensive test of these hypotheses, based on a trait-screening programme of 30 herbaceous crops and their wild progenitors. During crop evolution plants became larger, which enabled them to compete more effectively for light, but they had poorly integrated phenotypes. In a subset of six herbaceous crop species investigated in greater depth, competitiveness for light increased during early plant domestication, whereas diminished phenotypic integration occurred later during crop improvement. Mass-specific leaf and root traits relevant to resource-use strategies (e.g. specific leaf area or tissue density of fine roots) changed during crop evolution, but in diverse and contrasting directions and magnitudes, depending on the crop species. Reductions in phenotypic integration and overinvestment in traits involved in competition for light may affect the chances of upgrading modern herbaceous crops to face current climatic and food security challenges.

Shifts in stomatal traits following the domestication of plant species.

Stomata are the major gates regulating substrate availability for photosynthesis and water loss. Although both processes are critical to yield and to resource-use efficiency, we lack a comprehensive picture on how domestication and further breeding have impacted on leaf stomata. To fill this gap, stomatal sizes and densities were screened in cultivated and wild ancestor representatives of a uniquely large group of 24 herbaceous crops. Anatomical data and gas-exchange models were combined to compute maximum potential conductance to water, separately for upper and lower leaf sides. The evolution of maximum conductance under domestication was diverse. Several crops increased, others decreased (noticeably high-conductance species), and others kept a similar potential conductance following domestication. It was found that the contribution of upper leaf sides to maximum conductance was statistically higher in cultivated than in wild ancestors. For crops showing this response, reduced stomatal density in the lower side of domesticated leaves was responsible for the observed 'adaxialization' of conductance. Increases in the size of stomata at the upper epidermis played a comparatively minor role. Nevertheless, this overall response was varied in magnitude and direction, signalling crop-wise specificities. Observed patterns reflect only potential conductances based on anatomical traits and should be used with care until actual physiological outcomes are measured. Together with advancements in the developmental genetics of stomata, our findings might hint at new breeding avenues, focused on stomata distribution. Provided urgent needs for increasing yields, the opportunities of enhancing traits of the physiological relevance of stomata should not be ignored.

Side-effects of plant domestication: ecosystem impacts of changes in litter quality.

Domestication took plants from natural environments to agro-ecosystems, where resources are generally plentiful and plant life is better buffered against environmental risks such as drought or pathogens. We hypothesized that predictions derived from the comparison of low vs high resource ecosystems (faster-growing plants promoting faster nutrient cycling in the latter) extrapolate to the process of domestication. We conducted the first comprehensive assessment of the consequences of domestication on litter quality and key biogeochemical processes by comparing 24 domesticated crops against their closest wild ancestors. Twelve litter chemistry traits, litter decomposability and indicators of soil carbon (C) and nitrogen (N) cycling were assessed in each domesticated vs wild ancestor pair. These assessments were done in microbial-poor and microbial-rich soils to exemplify intensively and extensively managed agricultural soils, respectively. Plant domestication has increased litter quality, encouraging litter decomposability (36% and 44% increase in the microbial-rich and microbial-poor soils, respectively), higher soil NO3 - availability and lower soil C : N ratios. These effects held true for the majority of the crops surveyed and for soils with different microbial communities. Our results support ecological theory predictions derived from the comparison of low- and high-resource ecosystems, suggesting a parallelism between ecosystem-level impacts of natural and artificial selection.