Publications

Polymorphic genes of major effect: consequences for variation, selection and evolution in Arabidopsis thaliana

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Stinchcombe JR, Weinig C, Heath KD, Brock MT, Schmitt J

Genetics 2009 Jul;182(3):911-22

PubMed PMID: 19416942

Abstract

The importance of genes of major effect for evolutionary trajectories within and among natural populations has long been the subject of intense debate. For example, if allelic variation at a major-effect locus fundamentally alters the structure of quantitative trait variation, then fixation of a single locus can have rapid and profound effects on the rate or direction of subsequent evolutionary change. Using an Arabidopsis thaliana RIL mapping population, we compare G-matrix structure between lines possessing different alleles at ERECTA, a locus known to affect ecologically relevant variation in plant architecture. We find that the allele present at ERECTA significantly alters G-matrix structure-in particular the genetic correlations between branch number and flowering time traits-and may also modulate the strength of natural selection on these traits. Despite these differences, however, when we extend our analysis to determine how evolution might differ depending on the ERECTA allele, we find that predicted responses to selection are similar. To compare responses to selection between allele classes, we developed a resampling strategy that incorporates uncertainty in estimates of selection that can also be used for statistical comparisons of G matrices.

Evolution in plant populations as a driver of ecological changes in arthropod communities

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Johnson MT, Vellend M, Stinchcombe JR

Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2009 Jun;364(1523):1593-605

PubMed PMID: 19414473

Abstract

Heritable variation in traits can have wide-ranging impacts on species interactions, but the effects that ongoing evolution has on the temporal ecological dynamics of communities are not well understood. Here, we identify three conditions that, if experimentally satisfied, support the hypothesis that evolution by natural selection can drive ecological changes in communities. These conditions are: (i) a focal population exhibits genetic variation in a trait(s), (ii) there is measurable directional selection on the trait(s), and (iii) the trait(s) under selection affects variation in a community variable(s). When these conditions are met, we expect evolution by natural selection to cause ecological changes in the community. We tested these conditions in a field experiment examining the interactions between a native plant (Oenothera biennis) and its associated arthropod community (more than 90 spp.). Oenothera biennis exhibited genetic variation in several plant traits and there was directional selection on plant biomass, life-history strategy (annual versus biennial reproduction) and herbivore resistance. Genetically based variation in biomass and life-history strategy consistently affected the abundance of common arthropod species, total arthropod abundance and arthropod species richness. Using two modelling approaches, we show that evolution by natural selection in large O. biennis populations is predicted to cause changes in the abundance of individual arthropod species, increases in the total abundance of arthropods and a decline in the number of arthropod species. In small O. biennis populations, genetic drift is predicted to swamp out the effects of selection, making the evolution of plant populations unpredictable. In short, evolution by natural selection can play an important role in affecting the dynamics of communities, but these effects depend on several ecological factors. The framework presented here is general and can be applied to other systems to examine the community-level effects of ongoing evolution.

Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins

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Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR

Science 2009 May;324(5930):1068-71

PubMed PMID: 19407142

Abstract

Type 2C protein phosphatases (PP2Cs) are vitally involved in abscisic acid (ABA) signaling. Here, we show that a synthetic growth inhibitor called pyrabactin functions as a selective ABA agonist. Pyrabactin acts through PYRABACTIN RESISTANCE 1 (PYR1), the founding member of a family of START proteins called PYR/PYLs, which are necessary for both pyrabactin and ABA signaling in vivo. We show that ABA binds to PYR1, which in turn binds to and inhibits PP2Cs. We conclude that PYR/PYLs are ABA receptors functioning at the apex of a negative regulatory pathway that controls ABA signaling by inhibiting PP2Cs. Our results illustrate the power of the chemical genetic approach for sidestepping genetic redundancy.

Web-queryable large-scale data sets for hypothesis generation in plant biology

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Brady SM, Provart NJ

Plant Cell 2009 Apr;21(4):1034-51

PubMed PMID: 19401381

Abstract

The approaching end of the 21st century’s first decade marks an exciting time for plant biology. Several National Science Foundation Arabidopsis 2010 Projects will conclude, and whether or not the stated goal of the National Science Foundation 2010 Program-to determine the function of 25,000 Arabidopsis genes by 2010-is reached, these projects and others in a similar vein, such as those performed by the AtGenExpress Consortium and various plant genome sequencing initiatives, have generated important and unprecedented large-scale data sets. While providing significant biological insights for the individual laboratories that generated them, these data sets, in conjunction with the appropriate tools, are also permitting plant biologists worldwide to gain new insights into their own biological systems of interest, often at a mouse click through a Web browser. This review provides an overview of several such genomic, epigenomic, transcriptomic, proteomic, and metabolomic data sets and describes Web-based tools for querying them in the context of hypothesis generation for plant biology. We provide five biological examples of how such tools and data sets have been used to provide biological insight.

The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar

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Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP

Plant Physiol. 2009 Jun;150(2):924-41

PubMed PMID: 19395405

Abstract

In poplar (Populus spp.), the major defense phenolics produced in leaves are the flavonoid-derived proanthocyanidins (PAs) and the salicin-based phenolic glycosides. Transcriptional activation of PA biosynthetic genes leading to PA accumulation in leaves occurs following herbivore damage and mechanical wounding as well as infection by the fungal biotroph Melampsora medusae. In this study, we have identified a poplar R2R3 MYB transcription factor gene, MYB134, that exhibits close sequence similarity to the Arabidopsis (Arabidopsis thaliana) PA regulator TRANSPARENT TESTA2 and that is coinduced with PA biosynthetic genes following mechanical wounding, M. medusae infection, and exposure to elevated ultraviolet B light. Overexpression of MYB134 in poplar resulted in transcriptional activation of the full PA biosynthetic pathway and a significant plant-wide increase in PA levels, and electrophoretic mobility shift assays showed that recombinant MYB134 protein is able to bind to promoter regions of PA pathway genes. MYB134-overexpressing plants exhibited a concomitant reduction in phenolic glycoside concentrations and other minor alterations to levels of small phenylpropanoid metabolites. Our data provide insight into the regulatory mechanisms controlling stress-induced PA metabolism in poplar, and the identification of a regulator of stress-responsive PA biosynthesis constitutes a valuable tool for manipulating PA metabolism in poplar and investigating the biological functions of PAs in resistance to biotic and abiotic stresses.

Global robustness and identifiability of random, scale-free, and small-world networks

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Gong Y, Zhang Z

Ann. N. Y. Acad. Sci. 2009 Mar;1158:82-92

PubMed PMID: 19348634

Abstract

We are interested in the relationships among network topology, robustness, and identifiability, and their implications in improving network reconstruction. We used three different types of artificial gene networks (AGNs) with distinct topologies: topologies random (RND), scale-free (SF), and small-world (SW), to investigate their robustness and identifiability. The robustness of a network is represented by structural reachability (existence of pathways between two nodes) and dynamic reachability (response on one node upon perturbation on another node). The identifiability of the network edges is assessed in silico with an established reverse-engineering algorithm. We found that (1) structural reachability does not always lead to dynamic reachability; (2) network robustness is high and identifiability is low in all surveyed AGNs; (3) robustness is more sensitive to network topologies than is identifiability. We also devised a method for network dissection in which three subnets (set of alternative pathways or feedbacks, referred to as pathnet) are related to each node pair. This method allows us to identify the fine structural features underlying the distinct behaviors of the networks. For example, pathnet of the edge tail negatively contributes to the edge identifiability, and it is likely that extra perturbation at this pathnet would improve edge identifiability. We provide a case study to prove that double perturbations decrease the edge robustness and increase structural identifiability with a T helper cell-differentiation network model.

Neurogenic potential of isolated precursor cells from early post-gastrula somitic tissue

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Tropepe V, Alton K, Sachewsky N, Cheng V, Kuo C, Morshead CM

Stem Cells Dev. 2009 Dec;18(10):1533-42

PubMed PMID: 19326969

Abstract

Adult tissues are known to contain rare populations of stem cells with multilineage differentiation potential that are distinct from other resident tissue-specific stem cells. However, whether multilineage stem cells are involved in tissue development is uncertain, primarily because the identification and characterization of these cells in embryonic tissue primordia is not well established. We tested whether stem cells with multilineage potential are present within the early post-gastrula somite tissue. We show that clonally derived precursor cells generate colonies with self-renewal capacity and have both neurogenic and myogenic lineage potential. Somite colonies contain cells that express Sox2, nestin, and Sca1, but do not express genes indicative of somitic mesoderm specification. Furthermore, we demonstrate that this multilineage potential is not due to colony cells with a pluripotent epiblast identity or the selection of p75 receptor-positive neural crest stem cells. Despite utilizing a highly undifferentiated tissue source, colony formation was not enhanced relative to reported estimates of multilineage stem cells from adult muscle, a derivative of the embryonic somite. Thus, our findings suggest that a permissive in vitro environment is sufficient for the isolation of a discrete population of stem cells in the embryonic somite that may represent the earliest developmental precursor to adult muscle multilineage stem cells.

Evolution of the Caenorhabditis elegans genome

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Cutter AD, Dey A, Murray RL

Mol. Biol. Evol. 2009 Jun;26(6):1199-234

PubMed PMID: 19289596

Abstract

A fundamental problem in genome biology is to elucidate the evolutionary forces responsible for generating nonrandom patterns of genome organization. As the first metazoan to benefit from full-genome sequencing, Caenorhabditis elegans has been at the forefront of research in this area. Studies of genomic patterns, and their evolutionary underpinnings, continue to be augmented by the recent push to obtain additional full-genome sequences of related Caenorhabditis taxa. In the near future, we expect to see major advances with the onset of whole-genome resequencing of multiple wild individuals of the same species. In this review, we synthesize many of the important insights to date in our understanding of genome organization and function that derive from the evolutionary principles made explicit by theoretical population genetics and molecular evolution and highlight fertile areas for future research on unanswered questions in C. elegans genome evolution. We call attention to the need for C. elegans researchers to generate and critically assess nonadaptive hypotheses for genomic and developmental patterns, in addition to adaptive scenarios. We also emphasize the potential importance of evolution in the gonochoristic (female and male) ancestors of the androdioecious (hermaphrodite and male) C. elegans as the source for many of its genomic and developmental patterns.

Molecular evolution of the betagamma lens crystallin superfamily: evidence for a retained ancestral function in gamma N crystallins?

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Weadick CJ, Chang BS

Mol. Biol. Evol. 2009 May;26(5):1127-42

PubMed PMID: 19233964

Abstract

Within the vertebrate eye, betagamma crystallins are extremely stable lens proteins that are uniquely adapted to increase refractory power while maintaining transparency. Unlike alpha crystallins, which are well-characterized, multifunctional proteins that have important functions both in and out of the lens, betagamma lens crystallins are a diverse group of proteins with no clear ancestral or contemporary nonlens role. We carried out phylogenetic and molecular evolutionary analyses of the betagamma-crystallin superfamily in order to study the evolutionary history of the gamma N crystallins, a recently discovered, biochemically atypical family suggested to possess a divergent or ancestral function. By including nonlens, betagamma-motif-containing sequences in our analysis as outgroups, we confirmed the phylogenetic position of the gamma N family as sister to other gamma crystallins. Using maximum likelihood codon models to estimate lineage-specific nonsynonymous-to-synonymous rate ratios revealed strong positive selection in all of the early lineages within the betagamma family, with the striking exception of the lineage leading to the gamma N crystallins which was characterized by strong purifying selection. Branch-site analysis, used to identify candidate sites involved in functional divergence between gamma N crystallins and its sister clade containing all other gamma crystallins, identified several positively selected changes at sites of known functional importance in the betagamma crystallin protein structure. Further analyses of a fish-specific gamma N crystallin gene duplication revealed a more recent episode of positive selection in only one of the two descendant lineages (gamma N2). Finally, from the guppy, Poecilia reticulata, we isolated complete gamma N1 and gamma N2 coding sequence data from cDNA and partial coding sequence data from genomic DNA in order to confirm the presence of a novel gamma N2 intron, discovered through data mining of two pufferfish genomes. We conclude that the function of the gamma N family likely resembles the ancestral vertebrate betagamma crystallin more than other betagamma families. Furthermore, owing to the presence of an additional intron in some fish gamma N2 crystallins, and the inferred action of positive selection following the fish-specific gamma N duplication, we suggest that further study of fish gamma N crystallins will be critical in further elucidating possible ancestral functions of gamma N crystallins and any nonstructural role they may have.

Recent speciation associated with the evolution of selfing in Capsella

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Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI

Proc. Natl. Acad. Sci. U.S.A. 2009 Mar;106(13):5241-5

PubMed PMID: 19228944

Abstract

The evolution from outcrossing to predominant self-fertilization represents one of the most common transitions in flowering plant evolution. This shift in mating system is almost universally associated with the “selfing syndrome,” characterized by marked reduction in flower size and a breakdown of the morphological and genetic mechanisms that prevent self-fertilization. In general, the timescale in which these transitions occur, and the evolutionary dynamics associated with the evolution of the selfing syndrome are poorly known. We investigated the origin and evolution of selfing in the annual plant Capsella rubella from its self-incompatible, outcrossing progenitor Capsella grandiflora by characterizing multilocus patterns of DNA sequence variation at nuclear genes. We estimate that the transition to selfing and subsequent geographic expansion have taken place during the past 20,000 years. This transition was probably associated with a shift from stable equilibrium toward a near-complete population bottleneck causing a major reduction in effective population size. The timing and severe founder event support the hypothesis that selfing was favored during colonization as new habitats emerged after the last glaciation and the expansion of agriculture. These results suggest that natural selection for reproductive assurance can lead to major morphological evolution and speciation on relatively short evolutionary timescales.