Evolution of Plant Sexual Diversity

Abstract

Flowering plants possess striking sexual diversity despite the hermaphroditic condition of most species. Male and female gametes are deployed in a variety of spatial and temporal combinations at the flower, inflorescence and population level resulting in diverse sexual systems. As Darwin recognized, species with polymorphic sexual systems are especially valuable for evolutionary analysis, and studies of heterostyly and dioecy continue to provide key insights into evolutionary processes. Here, I provide an overview of our current work on the causes and genetic consequences of two of the most important evolutionary transitions in angiosperms: the pathway from outcrossing to predominant self-fertilization, and the origin of separate sexes (females and males) from hermaphroditism. The approaches used to address these problems include field studies of the ecology, demography and genetics of populations; comparative methods; genetic mapping of floral traits; and genomic and molecular evolutionary analyses.

The evolutionary breakdown of heterostyly to homostyly represents a classic system for investigating the shift from outcrossing to selfing. In Eichhornia this transition has occurred multiple times both within and among species. Evidence from E. paniculata indicates that the joint evolution of genetic drift and selection for reproductive assurance explains repeated transitions to selfing. Genotyping-by-sequencing and composite interval mapping of independently derived selfing forms that have colonized the Caribbean and Central America from Brazil, indicate that stamen modifications governing selfing occur on different linkage groups from the loci controlling tristyly. Each selfer has modifiers on a different linkage group consistent with their separate origins. This demonstrates that selfing can evolve via different genetic pathways within the same species. Transitions to selfing have resulted in a reduced efficacy of selection, the purging of deleterious mutations and changes in gene expression across the genome.

The transition from hermaphroditism to dioecy has occurred on multiple occasions in angiosperms. Although theory predicts 1:1 sex ratios in dioecious populations, biased ratios are common but the causes are not well understood. Our comparative analyses of angiosperms have revealed an association between heteromorphic sex chromosomes and female-biased sex ratios. In Rumex, a genus with heteromorphic sex chromosomes, natural populations often exhibit female-biased sex ratios and experimental studies have demonstrated that increased pollination intensity causes female bias. Moreover, theoretical work indicates that a balance between Fisherian sex-ratio selection and selection against deleterious mutations during the haploid phase can explain stable female biased sex ratios. These findings motivated us to investigate if the observed bias in populations is associated with Y-chromosome degeneration. Studies of sex-linked SNPs and transcriptome data have provided evidence of different degrees of Y-chromosome degeneration, depending on the time since recombination suppression, and a loss of neutral diversity consistent with selective interference among linked sites. Future comparative work on the genus will further investigate biased sex ratios, haploid selection and sex chromosome evolution across the phylogeny. Collectively, these studies of two polymorphic sexual systems both highlight the important genomic consequences of recombination suppression and also the insights that can be gained from intraspecific studies or natural variation.

Applications of genomics to crop plant improvement

Abstract

Recent advances in genome sequencing technologies, coupled to radically improved assembly and annotation methods, have revolutionized genomics. These approaches are now being used to tackle crop plants with large and complex polyploid genomes. New methods for sequencing populations of crop plants and their wild relatives are also providing unprecedented access to a wide range of genetic variation. In my presentation I will use the wheat genome as an example of such progress.  The question now is how can genomics guide and accelerate the breeding and engineering of crops with improved characteristics. I will provide examples of how our research teams at the John Innes Centre and the Earlham Institute in the UK are going about delivering the great promise of genomics. 

On the exceptional value of model lineages in systematics and comparative biology

Abstract

With reference to a model portraying the scope of systematics and comparative biology, I will argue that comprehensive analyses of model lineages have a critical role to play in advancing our understanding of plants and their evolution.  Such studies provide new avenues for analyzing how organisms are integrated and the evolutionary causes and consequences of this integration.  They also provide a sound basis for the comparative analyses that are most likely to yield insights of lasting significance.  As a concrete example I will highlight our ongoing studies of the angiosperm clade Viburnum (Adoxaceae).  Specifically, I will develop connections between our analyses of leaf structure, function and evolution in Viburnum and global patterns in leaf form and leafing habit.  These studies identify new traits of potential interest in studies of global change. 

Fertilization Mechanisms: A Comparison of Eudicots and Grasses

Abstract

Cell Biology and Plant Biochemistry, Biochemie-Zentrum Regensburg, University of Regensburg, 93053 Regensburg, Germany

After leaving their aquatic environment land plants adapted to various environmental challenges and evolved specialized reproductive structures. Originally, their sperm cells were motile and capable to swim to egg cells. This mode of fertilization is still preserved in most mosses and ferns preferring moist environments. However, flowering plants or angiosperms, which dominate in colder and dryer habitats, evolved embedded gametophytes to protect egg and immobile sperm cells. Male gametophytes or pollen grains develop in anthers, while female gametophytes or embryo sacs are produced deeply inside the maternal tissues of ovule and ovary, respectively. After release pollen grains of angiosperms are transported by wind or animals to female flower organs of the same species. They germinate, penetrate stigmatic tissue and grow through the style towards the ovule to deliver their passive sperm cell cargo. Inside the female gametophyte double fertilization is executed resulting in embryo and endosperm formation, respectively. To avoid fertilization failures and to promote outcrossing, angiosperms have developed various mechanisms to distinguish between own and alien pollen as well as pollen of the own species. Using Arabidopsis as a eudicot and maize as a grass model, I will compare morphological differences and focus on similar and distinct molecular mechanisms associated to fertilization. These include various hurdles along the pollen tube pathway, during sperm cell release and gamete activation. The analysis of genes involved in pollen adhesion, hydration and penetration, pollen tube growth and guidance as well as double fertilization and onset of embryo development will be presented. Some genes with key functions for fertilization and egg activation in maize lack homologs in Arabidopsis, while other genes are highly polymorphic. Molecular systems to discriminate own and foreign tubes will be presented and possibilities discussed to generate a new species.

Deconstructing the Plant Regulatory Genome: Enabling Technologies

Abstract

Genetic and epigenetic variation can impact gene transcription and phenotypic diversity and may thus contribute to adaptation. We have produced and characterized  > 1000 high quality single-base resolution genomes, methylomes, and transcriptomes from a global collection of Arabidopsis thaliana ecotypes/accessions. Although the genetic basis of methylation variation is highly complex, geographic origin is a major predictor of global DNA methylation levels and altered gene expression caused by epialleles. Analysis of the cistromes and epicistromes of these 1001 accessions revealed significant association between transcription factor binding (TF) sites, methylation and nucleotide variation and co-expression modules. To more directly interrogate the effects of genetic and epigenetic variation on TF binding, we developed a high-throughput TF binding site discovery method and defined the Arabidopsis cistrome by resolving motifs and peaks for a large number of TFs. We have also developed a massively multiple yeast 2-hybrid based method for studies of protein:protein interactions and applied this approach to study of Arabidopsis TF:TF interactions. These approaches are advancing our understanding of how both genetic and epigenetic variation contribute to phenotype in natural populations.

1001 Genomes Consortium. 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell. 2016 Jul 14;166(2):481-91. doi: 10.1016/j.cell.2016.05.063. Epub 2016 Jun 9. PubMed PMID: 27293186; PubMed Central PMCID: PMC4949382.

Kawakatsu T, Huang SS, Jupe F, Sasaki E, Schmitz RJ, Urich MA, Castanon R, Nery JR, Barragan C, He Y, Chen H, Dubin M, Lee CR, Wang C, Bemm F, Becker C, O'Neil R, O'Malley RC, Quarless DX; 1001 Genomes Consortium, Schork NJ, Weigel D, Nordborg M, Ecker JR. Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions. Cell. 2016 Jul 14;166(2):492-505. doi:10.1016/j.cell.2016.06.044. PubMed PMID: 27419873. 

O'Malley RC, Huang SS, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR. Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell. 2016 May 19;165(5):1280-92. doi: 10.1016/j.cell.2016.04.038. PubMed PMID: 27203113; PubMed Central PMCID: PMC4907330.

Structural characteristics of forests and diversity of woody plants in China

Abstract

China is rich in forest communities and woody plants. To systematically investigate species composition and structure of China’s forest communities, we launched a long-term project consisting forest vegetation surveys across China’s mountains in the mid 1990s. Over the study period, we have conducted vegetation surveys for more than 70 mountains and collected vegetation data from about 2000 forest plots, using consistent sampling protocols. Meanwhile, to explore geographic patterns and their environmental controls of woody species diversity, we established a huge database of distribution of China’s woody plants that contains all 11405 woody species in the country. Our results indicated that as latitude increased, diameter at breast height (DBH) and height of trees increased, while individual density of trees and woody species richness decreased. Total basal area (TBA) of trees and species richness of herbs did not vary with latitude. Contemporary climate seems to drive these patterns: temperature was the leading factor for DBH, precipitation was most important for tree height and individual density, actual evapotranspiration (a surrogate of productivity) determined woody (trees and shrubs) species richness, and rainfall was the major controller of the herb species richness. The species–abundance relationship showed that species dominance (measured by the number of individuals per species) declined significantly from boreal forests to evergreen broadleaf forests from north to south. Further, using the database of distribution of woody plants, we compared the effects of habitat heterogeneity, human activities and climatic variables (particularly environmental energy, water–energy dynamics and winter frost) on the woody species diversity, and found that the contemporary climate explained the spatial variation of more than 80%, of which winter mean temperature of the coldest quarter was the strongest predictor, thus supporting the freezing-tolerance hypothesis.

Understanding the molecular basis of rice plant architecture

Abstract

Rice is the most important staple crop in China and an ideal model plant. How to increase yield and improve quality has been the major challenge in rice research and breeding. However, to meet the security of food supply, the crop yield per unit area has to be increased by 50% before 2030. My lab has been focused on systematical dissection of key genes regulating rice plant architecture, elucidation of their molecular mechanisms and the genetic regulatory network, and application of this fundamental knowledge to breed new high-yield elite varieties.

Plant architecture is a primary determinant of crop yield and has profound adaptability in response to internal and external factors. Research on rice plant architecture and understanding of the molecular basis and regulatory mechanism are of great importance to both basic science and practical application. Plant architecture is mainly determined by plant height, tiller number, tiller angle and panicle morphology. My lab has molecularly characterized a series of rice mutants that show various altered plant tillering or panicle phenotypes, including monoclum 1 (moc1), tillering and dwarf 1 (tad1), ideal plant architecture 1 (ipa1), lazy1 (la1), small panicle 1 (sp1), dwarf 27 (d27), and dwarf 53 (d53). We cloned these corresponding genes through map-based cloning approaches and in-depth characterization of their functions, demonstrating that the tillering phenotypes mainly result from either the deficiency in the branching plant hormone strigolactone biosynthetic and signaling pathways or the transcription factors that play key roles in plant architecture formation. The understanding of these gene functions enable us to elucidate a comprehensive regulatory network underlying the formation of plant architecture and greatly expanded our knowledge of plant development.

Based on the knowledge from the study on plant architecture of rice, our lab and collaborators have made enormous efforts in breeding new elite varieties through developing a molecular breeding system. These results demonstrate that this system could truly speed up the rice breeding course and generate new super rice with multiple advantages. However, to fully meet the challenge of food supply, more efforts need to be made by providing more genetic resources and designing different allele combinations to meet the unique demands in different regions in China.

Keywords: Plant architecture, molecular breeding by design, rice

Computational Morphodynamic Approaches to Pattern Formation in the Shoot Apical Meristem of Arabidopsis

Abstract

The shoot apical meristem is the stem cell niche responsible for generating the above-ground parts of flowering plants, including stems, leaves and flowers.  Though only a few hundred cells, it has a large number of overlapping but different domains of gene expression. These gene expression domains are dynamic – some genes change their expression relative to appearance of new leaf or flower primordia. Others are expressed in what appear to be stable domains in the meristem – but are not stable, as the cells that express the genes are dividing, and some progeny cells enter these domains as others depart, making them dynamic at the cellular level, even though stable in comparison to the meristem boundaries.  How are these gene expression patterns controlled?  By iteration between computational models of cell-cell interactions, and experiments to test the models, we have developed robust hypotheses for flower primordium-influenced gene expression that involve interactions between chemical (auxin) and mechanical signals in the meristem, and for meristem region-specific expression we have models where cell-cell communication is mediated by a combination of small-molecule (cytokinin) and peptide signals.

The origin of economically important species of Cucumis, Citrullus, and Momordica – combining Chinese genomics know-how and old European herbaria to find wild relatives

Abstract

China is World-leading in Cucurbitaceae genomics, having produced the draft genomes of cucumber,

China is World-leading in Cucurbitaceae genomics, having produced the draft genomes of cucumber, Cucumis sativus (Huang et al., Nature Genetics 2009; also Qi et al., Nature Genetics, 2013; Shang et al., Science 2014; Zhou et al., Nature Plants 2016) and watermelon, Citrullus ‘lanatus’ (Guo et al., Nature Genetics 2013). Old-fashioned Sanger sequencing over the past 10 years, however, has revealed numerous misclassifications of material of Cucurbitaceae, from simple misidentification of germplasm to serious misplacements of species in unnatural genera, meaning that names do not reflect evolutionary relationships and cannot be trusted to guide sampling for genomic projects. The family Cucurbitaceae is underrepresented in herbaria because wild cucurbits often are climbers in disturbed habitats or desert plants that are hard to find at the right stage. Fruits of the family are difficult to preserve. Only with DNA barcoding has it become possible to figure out what is what (simply put). In the talk I will illustrate how molecular data are revolutionizing our knowledge about the wild relatives of Cucumis sativus (in India, Thailand, and tropical China), Cucumis melo (in India and Australia), Citrullus lanatus (in West or Northeast Africa), Momordica charantia (in Africa) and Luffa (in India and Australia), using examples of recent and ongoing work in my lab, in collaboration with genomics experts from China.

EXAMPLES:

Renner, S. S., H. Schaefer, and A. Kocyan. 2007. Phylogenetics of Cucumis (Cucurbitaceae): Cucumber (C. sativus) belongs in an Asian/Australian clade far from melon (C. melo). BMC Evolutionary Biology 7:58. DOI: 10.1186/1471-2148-7-58 (“highly accessed”)

Schaefer, H., C. Heibl, and S. S. Renner. 2009. Gourds afloat: A dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proceedings of the Royal Society B 276 (1658): 843-851.

Schaefer, H., and S. S. Renner. 2010. A three-genome phylogeny of Momordica (Cucurbitaceae) suggests seven returns from dioecy to monoecy and recent long-distance dispersal to Asia. Molecular Phylogenetics and Evolution 54(2): 553-560.

Sebastian, P. M., H. Schaefer, I. R. H. Telford, and S. S. Renner. 2010. Cucumber and melon have their wild progenitors in India, and the sister species of Cucumis melo is from Australia. Proceedings of the National Academy of Sciences, USA 107(32): 14269–14273.  

Chomicki, G., and S. S. Renner. 2015. Watermelon origin solved with molecular phylogenetics including Linnaean material: Another example of museomics. New Phytologist 205(2): 526-532.

Plant Evolution in the Anthropocene

Abstract

Humans have emerged as the dominant selective force on our planet.  This provides unparalleled opportunities for evolutionary biologists to study evolution in action.  However, it also leads to the question of whether plants (and other organisms) can evolve fast enough to keep up with the rapid pace of human-caused environmental change. I will discuss what we have learned about plant adaptation and speciation from studies of contemporary evolution.  Plant evolution in the Anthropocene is pervasive and can be rapid, but in many species it lags behind environmental change due to long generation times and limited dispersal.  In the absence of intervention, extinction of such taxa seems likely.  To maintain productive communities and ecosystems, plant biologists must develop strategies to aid adaptation when desired (e.g., evolving climate-adapted crops or forests) and hinder it when necessary (e.g., in weeds).  More generally, our focus going forward should be on adaptation rather than preservation of the status quo.

Linking Heterogeneous Data in Botanical Research

Abstract

Plant diversity is the product of complex interrelationships among genetics, ecology, and evolution, yet integration of these disciplines of botanical research remains elusive.

Emerging cyberinfrastructure and new data sources provide unparalleled opportunities for mobilizing and integrating massive amounts of information from organismal biology, ecology, genetics, phylogenetics, climatology, and other disciplines.  Key among these data sources is the rapidly growing volume of digitized specimen records from natural history collections.  With nearly 100 million specimen records currently publically available online, these data provide excellent information on species distributions and changes in phenology and distributions over time.  Particularly powerful is the integration of phylogenies with specimen data, enabling analyses of phylogenetic diversity in a spatio-temporal context, the evolution of niche space, and more, while phylogenomic analyses that synthesize phylogenies and genome-scale data shed new light on the role of genomic change in plant diversification.  The burgeoning field of phenomics offers still further data for integration with phylogenetic, genomic, and ecological data.  However, a major challenge to synthetic research is the heterogeneous nature of complex data, and new methods are needed to link these divergent data types.  Ongoing efforts to link and analyze diverse data are yielding new perspectives on a range of evolutionary and ecological problems.  We will present multiple case studies that attempt to integrate heterogeneous data sources in analyses of plant diversity.  Although many specific hypotheses may be addressed through integrated analyses of linked biodiversity and environmental data, additional value of such data-enabled science lies in the unanticipated patterns that emerge.

Decoding the epigenetic language of life

Abstract

Epigenetics refers to the study of heritable information that is not contained in DNA sequence. An important epigenetic mark conserved in mammals and plants is DNA methylation, a chemical modification of DNA that controls gene function. Proper DNA methylation patterns are critical for development, diseases and stress responses in humans as well as in plants. Plants are excellent biological systems to study how DNA methylation patterns are generated. DNA methyltransferase enzymes that deposit the DNA methylation mark are guided to specific DNA sequences, and DNA demethylase enzymes that remove the DNA methylation mark are also guided to distinctive sequences to erase unwanted DNA methylation. I will describe work in my lab that has shed light on how DNA methyltransferases and demethylases are guided to specific sequences, and how the antagonistic actions of the enzymes are coordinated to generate proper DNA methylation patterns. I will also describe some of our recent work on how DNA methylation influences transgenerational inheritance.