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In plant communities, diversity often increases productivity and functioning, but the specific underlying drivers are difficult to identify. Most ecological theories attribute positive diversity effects to complementary niches occupied by different species or genotypes. However, the specific nature of niche complementarity often remains unclear, including how it is expressed in terms of trait differences between plants. Here, we use a gene-centred approach to study positive diversity effects in mixtures of natural Arabidopsis thaliana genotypes. Using two orthogonal genetic mapping approaches, we find that between-plant allelic differences at the AtSUC8 locus are strongly associated with mixture overyielding. AtSUC8 encodes a proton-sucrose symporter and is expressed in root tissues. Genetic variation in AtSUC8 affects the biochemical activities of protein variants and natural variation at this locus is associated with different sensitivities of root growth to changes in substrate pH. We thus speculate that - in the particular case studied here - evolutionary divergence along an edaphic gradient resulted in the niche complementarity between genotypes that now drives overyielding in mixtures. Identifying genes important for ecosystem functioning may ultimately allow linking ecological processes to evolutionary drivers, help identify traits underlying positive diversity effects, and facilitate the development of high-performance crop variety mixtures.

Historic yield advances in the major crops have, to a large extent, been achieved by selection for improved productivity of groups of plant individuals such as high-density stands. Research suggests that such improved group productivity depends on “cooperative” traits (e.g., erect leaves, short stems) that—while beneficial to the group—decrease individual fitness under competition. This poses a problem for some traditional breeding approaches, especially when selection occurs at the level of individuals, because “selfish” traits will be selected for and reduce yield in high-density monocultures. One approach, therefore, has been to select individuals based on ideotypes with traits expected to promote group productivity. However, this approach is limited to architectural and physiological traits whose effects on growth and competition are relatively easy to anticipate. Here, we developed a general and simple method for the discovery of alleles promoting cooperation in plant stands. Our method is based on the game-theoretical premise that alleles increasing cooperation benefit the monoculture group but are disadvantageous to the individual when facing noncooperative neighbors. Testing the approach using the model plant Arabidopsis thaliana, we found a major effect locus where the rarer allele was associated with increased cooperation and productivity in high-density stands. The allele likely affects a pleiotropic gene, since we find that it is also associated with reduced root competition but higher resistance against disease. Thus, even though cooperation is considered evolutionarily unstable except under special circumstances, conflicting selective forces acting on a pleiotropic gene might maintain latent genetic variation for cooperation in nature. Such variation, once identified in a crop, could rapidly be leveraged in modern breeding programs and provide efficient routes to increase yields.

Historic yield advances in the major crops have, to a large extent, been achieved by selection for improved productivity of groups of plant individuals such as high-density stands. Research suggests that such improved group productivity depends on “cooperative” traits (e.g., erect leaves, short stems) that—while beneficial to the group—decrease individual fitness under competition. This poses a problem for some traditional breeding approaches, especially when selection occurs at the level of individuals, because “selfish” traits will be selected for and reduce yield in high-density monocultures. One approach, therefore, has been to select individuals based on ideotypes with traits expected to promote group productivity. However, this approach is limited to architectural and physiological traits whose effects on growth and competition are relatively easy to anticipate. Here, we developed a general and simple method for the discovery of alleles promoting cooperation in plant stands. Our method is based on the game-theoretical premise that alleles increasing cooperation benefit the monoculture group but are disadvantageous to the individual when facing noncooperative neighbors. Testing the approach using the model plant Arabidopsis thaliana, we found a major effect locus where the rarer allele was associated with increased cooperation and productivity in high-density stands. The allele likely affects a pleiotropic gene, since we find that it is also associated with reduced root competition but higher resistance against disease. Thus, even though cooperation is considered evolutionarily unstable except under special circumstances, conflicting selective forces acting on a pleiotropic gene might maintain latent genetic variation for cooperation in nature. Such variation, once identified in a crop, could rapidly be leveraged in modern breeding programs and provide efficient routes to increase yields.

Establishing the embryonic body plan of multicellular organisms relies on precisely orchestrated cell divisions coupled with pattern formation, which, in animals, are regulated by Polycomb group (PcG) proteins. The conserved Polycomb Repressive Complex 2 (PRC2) mediates H3K27 trimethylation and comes in different flavors in Arabidopsis. The PRC2 catalytic subunit MEDEA is required for seed development; however, a role for PRC2 in embryonic patterning has been dismissed. Here, we demonstrate that embryos derived from medea eggs abort because MEDEA is required for patterning and cell lineage determination in the early embryo. Similar to PcG proteins in mammals, MEDEA regulates embryonic patterning and growth by controlling cell-cycle progression through repression of CYCD1;1, which encodes a core cell-cycle component. Thus, Arabidopsis embryogenesis is epigenetically regulated by PcG proteins, revealing that the PRC2-dependent modulation of cell-cycle progression was independently recruited to control embryonic cell proliferation and patterning in animals and plants.

Establishing the body plan of a multicellular organism relies on precisely orchestrated cell divisions coupled with pattern formation. In animals, cell proliferation and embryonic patterning are regulated by Polycomb group (PcG) proteins that form various multisubunit complexes (Grossniklaus and Paro, 2014). The evolutionary conserved Polycomb Repressive Complex 2 (PRC2) trimethylates histone H3 at lysine 27 (H3K27me3) and comes in different flavors in the model plant Arabidopsis thaliana (Förderer et al., 2016; Grossniklaus and Paro, 2014). The histone methyltransferase MEDEA (MEA) is part of the FERTILIZATION INDEPENDENT SEED (FIS)-PRC2 required for seed development4. Although embryos derived from mea mutant egg cells show morphological abnormalities (Grossniklaus et al., 1998), defects in the development of the placenta-like endosperm are considered the main cause of seed abortion (Kinoshita et al., 1999; Scott et al., 1998), and a role of FIS-PRC2 in embryonic patterning was dismissed (Bouyer et al., 2011; Leroy et al., 2007). Here, we demonstrate that endosperm lacking MEA activity sustains normal embryo development and that embryos derived from mea mutant eggs abort even in presence of a wild-type endosperm because MEA is required for embryonic patterning and cell lineage determination. We show that, similar to PcG proteins in mammals, MEA regulates embryonic growth by repressing the transcription of core cell cycle components. Our work demonstrates that Arabidopsis embryogenesis is under epigenetic control of maternally expressed PcG proteins, revealing that PRC2 was independently recruited to control embryonic cell proliferation and patterning in animals and plants.

Technologies for crop breeding have become increasingly sophisticated, yet it remains unclear whether these advances are sufficient to meet future demands. A major challenge with current crop selection regimes is that they are often based on individual performance. This tends to select for plants with “selfish” traits, which leads to a yield loss when they compete in high-density stands. In traditional breeding, this well-known “tragedy of the commons” has been addressed by anticipating ideotypes with presumably preferential characteristics. However, this approach is limited to obvious architectural and physiological traits, and it depends on a mechanistic understanding of how these modulate growth and competition. Here, we developed a general and simple method for the discovery of alleles promoting cooperation of plants in stands; it is based on the game-theoretical premise that alleles increasing cooperation incur a cost to the individual but benefit the monoculture group. Testing the approach using the model plant Arabidopsis thaliana, we found a single major effect locus where the rarer allele was associated with increased levels of cooperation and superior monoculture productivity. We show that the allele likely affects a pleiotropic regulator of growth and defense, since it is also associated with reduced root competition but higher race-specific resistance against a specialized parasite. Even though cooperation is considered evolutionarily unstable, conflicting selective forces acting on a pleiotropic gene might thus maintain latent genetic variation for it in nature. Such variation, once identified in a crop, could be rapidly leveraged in modern breeding programs and provide efficient routes to increase yields.

The epithelial-to-mesenchymal transition (EMT) is an important mechanism for cancer progression and metastasis. Numerous in vitro and tumor-profiling studies point to the miR-200–Zeb1 axis as crucial in regulating this process, yet in vivo studies involving its regulation within a physiological context are lacking. Here, we show that miR-200 ablation in the Rip-Tag2 insulinoma mouse model induces beta-cell dedifferentiation, initiates an EMT expression program, and promotes tumor invasion. Strikingly, disrupting the miR-200 sites of the endogenous Zeb1 locus causes a similar phenotype. Reexpressing members of the miR-200 superfamily in vitro reveals that the miR-200c family and not the co-expressed and closely related miR-141 family is responsible for regulation of Zeb1 and EMT. Our results thus show that disrupting the in vivo regulation of Zeb1 by miR-200c is sufficient to drive EMT, thus highlighting the importance of this axis in tumor progression and invasion and its potential as a therapeutic target., National Institute of General Medical Sciences (U.S.)

Parent-of-origin effects play important roles in plant reproduction and are often mediated by epigenetic modifications at the histone or DNA level. However, the genetic basis underlying these modifications can be challenging to identify. Here, we describe an approach (Bulk-Seq) that can be used to map loci mediating parent-of-origin-dependent effects using whole-genome sequencing of pools of DNA.

Seeds are multi-generational structures containing a small embryonic plant enclosed in layers of diverse parental origins. The evolution of seeds was a pinnacle in an evolutionary trend towards a progressive retention of embryos and gametes within parental tissue. This strategy, which dates back to the first land plants, allowed an increased protection and nourishing of the developing embryo. Flowering plants took parental control one step further with the evolution of a biparental endosperm that derives from a second parallel fertilization event. The endosperm directly nourishes the developing embryo and allows not only the maternal genes, but also paternal genes, to play an active role during seed development. The appearance of an endosperm set the conditions for the manifestation of conflicts of interest between maternal and paternal genomes over the allocation of resources to the developing embryos. As a consequence, a dynamic balance was established between maternal and paternal gene dosage in the endosperm, and maintaining a correct balance became essential to ensure a correct seed development. This balance was achieved in part by changes in the genetic constitution of the endosperm and through epigenetic mechanisms that allow a differential expression of alleles depending on their parental origin. This review discusses the evolutionary steps that resulted in the appearance of seeds and endosperm, and the epigenetic and genetic mechanisms that allow a harmonious coinhabitance of multiple generations within a single seed

Embryonic development requires a correct balancing of maternal and paternal genetic information. This balance is mediated by genomic imprinting, an epigenetic mechanism that leads to parent-of-origin-dependent gene expression. The parental conflict (or kinship) theory proposes that imprinting can evolve due to a conflict between maternal and paternal alleles over resource allocation during seed development. One assumption of this theory is that paternal alleles can regulate seed growth; however, paternal effects on seed size are often very low or non-existent. We demonstrate that there is a pool of cryptic genetic variation in the paternal control of Arabidopsis thaliana seed development. Such cryptic variation can be exposed in seeds that maternally inherit a medea mutation, suggesting that MEA acts as a maternal buffer of paternal effects. Genetic mapping using recombinant inbred lines, and a novel method for the mapping of parent-of-origin effects using whole-genome sequencing of segregant bulks, indicate that there are at least six loci with small, paternal effects on seed development. Together, our analyses reveal the existence of a pool of hidden genetic variation on the paternal control of seed development that is likely shaped by parental conflict.

Species-specific gamete recognition is a key premise to ensure reproductive success and the maintenance of species boundaries. During plant pollen tube (PT) reception, gametophyte interactions likely allow the species-specific recognition of signals from the PT (male gametophyte) by the embryo sac (female gametophyte), resulting in PT rupture, sperm release, and double fertilization. This process is impaired in interspecific crosses between Arabidopsis thaliana and related species, leading to PT overgrowth and a failure to deliver the sperm cells. Here we show that ARTUMES (ARU) specifically regulates the recognition of interspecific PTs in A. thaliana. ARU, identified in a genome-wide association study (GWAS), exclusively influences interspecific--but not intraspecific--gametophyte interactions. ARU encodes the OST3/6 subunit of the oligosaccharyltransferase complex conferring protein N-glycosylation. Our results suggest that glycosylation patterns of cell surface proteins may represent an important mechanism of gametophyte recognition and thus speciation.

Embryonic development requires a correct balancing of maternal and paternal genetic information. This balance is mediated by genomic imprinting, an epigenetic mechanism that leads to parent-of-origin-dependent gene expression. The parental conflict (or kinship) theory proposes that imprinting can evolve due to a conflict between maternal and paternal alleles over resource allocation during seed development. One assumption of this theory is that paternal alleles can regulate seed growth; however, paternal effects on seed size are often very low or non-existent. We demonstrate that there is a pool of cryptic genetic variation in the paternal control of Arabidopsis thaliana seed development. Such cryptic variation can be exposed in seeds that maternally inherit a medea mutation, suggesting that MEA acts as a maternal buffer of paternal effects. Genetic mapping using recombinant inbred lines, and a novel method for the mapping of parent-of-origin effects using whole-genome sequencing of segregant bulks, indicate that there are at least six loci with small, paternal effects on seed development. Together, our analyses reveal the existence of a pool of hidden genetic variation on the paternal control of seed development that is likely shaped by parental conflict.

Seeds are multi-generational structures containing a small embryonic plant enclosed in layers of diverse parental origins. The evolution of seeds was a pinnacle in an evolutionary trend towards a progressive retention of embryos and gametes within parental tissue. This strategy, which dates back to the first land plants, allowed an increased protection and nourishing of the developing embryo. Flowering plants took parental control one step further with the evolution of a biparental endosperm that derives from a second parallel fertilization event. The endosperm directly nourishes the developing embryo and allows not only the maternal genes, but also paternal genes, to play an active role during seed development. The appearance of an endosperm set the conditions for the manifestation of conflicts of interest between maternal and paternal genomes over the allocation of resources to the developing embryos. As a consequence, a dynamic balance was established between maternal and paternal gene dosage in the endosperm, and maintaining a correct balance became essential to ensure a correct seed development. This balance was achieved in part by changes in the genetic constitution of the endosperm and through epigenetic mechanisms that allow a differential expression of alleles depending on their parental origin. This review discusses the evolutionary steps that resulted in the appearance of seeds and endosperm, and the epigenetic and genetic mechanisms that allow a harmonious coinhabitance of multiple generations within a single seed.

The evolution of multicellular organisms was made possible by the evolution of underlying gene regulatory networks. In animals, the core of gene regulatory networks consists of kernels, stable subnetworks of transcription factors that are highly conserved in distantly related species. However, in plants it is not clear when and how kernels evolved. We show here that RSL (ROOT HAIR DEFECTIVE SIX-LIKE) transcription factors form an ancient land plant kernel controlling caulonema differentiation in the moss Physcomitrella patens and root hair development in the flowering plant Arabidopsis thaliana. Phylogenetic analyses suggest that RSL proteins evolved in aquatic charophyte algae or in early land plants, and have been conserved throughout land plant radiation. Genetic and transcriptional analyses in loss of function A. thaliana and P. patens mutants suggest that the transcriptional interactions in the RSL kernel were remodeled and became more hierarchical during the evolution of vascular plants. We predict that other gene regulatory networks that control development in derived groups of plants may have originated in the earliest land plants or in their ancestors, the Charophycean algae.

Seeds are multi-generational structures containing a small embryonic plant enclosed in layers of diverse parental origins. The evolution of seeds was a pinnacle in an evolutionary trend towards a progressive retention of embryos and gametes within parental tissue. This strategy, which dates back to the first land plants, allowed an increased protection and nourishing of the developing embryo. Flowering plants took parental control one step further with the evolution of a biparental endosperm that derives from a second parallel fertilization event. The endosperm directly nourishes the developing embryo and allows not only the maternal genes, but also paternal genes, to play an active role during seed development. The appearance of an endosperm set the conditions for the manifestation of conflicts of interest between maternal and paternal genomes over the allocation of resources to the developing embryos. As a consequence, a dynamic balance was established between maternal and paternal gene dosage in the endosperm, and maintaining a correct balance became essential to ensure a correct seed development. This balance was achieved in part by changes in the genetic constitution of the endosperm and through epigenetic mechanisms that allow a differential expression of alleles depending on their parental origin. This review discusses the evolutionary steps that resulted in the appearance of seeds and endosperm, and the epigenetic and genetic mechanisms that allow a harmonious coinhabitance of multiple generations within a single seed