Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea

Two patterns of plant defense gene evolution are emerging from molecular population genetic surveys. One is that specialist defenses experience stronger selection than generalist defenses. The second is that specialist defenses are more likely to be subject to balancing selection, i.e., evolve in a manner consistent with balanced-polymorphism or trench-warfare models of host-parasite coevolution. Because most of the data of specialist defenses come from Arabidopsis thaliana, we examined the genetic diversity and evolutionary history of three defense genes in two outcrossing species, the autotetraploid Zea perennis and its most closely related extant relative the diploid Z. diploperennis. Intraspecific diversity at two generalist defenses, the protease inhibitors wip1 and mpi, were consistent with a neutral model. Like previously studied genes in these taxa, wip1 and mpi harbored similar levels of diversity in Z. diploperennis and Z. perennis. In contrast, the specialist defense hm2 showed strong although distinctly different departures from a neutral model in the two species. Z. diploperennis appears to have experienced a strong and recent selective sweep. Using a rejection-sampling coalescent method, we estimate the strength of selection on Z. diploperennis hm2 to be approximately 3.0%, which is approximately equal to the strength of selection on tb1 during maize domestication. Z. perennis hm2 harbors three highly diverged alleles, two of which are found at high frequency. The distinctly different patterns of diversity may be due to differences in the phase of host-parasite coevolutionary cycles, although higher hm2 diversity in Z. perennis may also reflect reduced efficacy of selection in the autotetraploid relative to its diploid relative.     

Higher expression of induced defenses in teosintes (Zea spp.) is correlated with greater resistance to fall armyworm,Spodoptera frugiperda

Selection for plant traits important for agriculture can come at a high cost to plant defenses. While selecting for increased growth rate and yield, domestication and subsequent breeding may lead to weakened defenses and greater susceptibility of plants to herbivores. We tested whether expression of defense genes differed among maize, Zea mays ssp. mays L. (Poaceae), and its wild relatives Zea mays ssp. parviglumis Iltis & Doebley and Zea diploperennis Iltis et al. We used two populations of Z. mays ssp. parviglumis: one expected to express high levels of an herbivore resistance gene, wound‐inducible protein (wip1), and another expected to have low expression of wip1. To test whether maize and wild Zea differed in induction of defenses against Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), we quantified expression of several genes involved in plant defense: wip1, maize protease inhibitor (mpi), pathogenesis‐related protein (PR‐1), and chitinase. Moreover, we compared growth, development, and survival of caterpillars on maize and wild Zea plants. We found that maize expressed low levels of all but one of the genes when attacked by caterpillars, whereas the wild relatives of maize expressed induced defense genes at high levels. Expression of wip1, in particular, was much greater in the Z. mays ssp. parviglumis population that we expected to naturally express high levels of wip1, with expression levels 29‐fold higher than in herbivore‐free plants. Elevated expression of defenses in wild plants was correlated with higher resistance to caterpillars. Larvae were 15–20% smaller on wild Zea compared with maize, developed 20% slower, and only 22% of them survived to pupation on Z. mays ssp. parviglumis with high levels of wip1. Our results suggest that domestication has inadvertently reduced the resistance of maize, and it is likely that expression of wip1 and other genes associated with defenses play an important role in this reduction in resistance.     

Population genetics of duplicated disease-defense genes,hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis)

Plant defense genes are subject to nonneutral evolutionary dynamics. Here we investigate the evolutionary dynamics of the duplicated defense genes hm1 and hm2 in maize and its wild ancestor Zea mays ssp. parviglumis. Both genes have been shown to confer resistance to the fungal pathogen Cochliobolus carbonum race 1, but the effectiveness of resistance differs between loci. The genes also display different population histories. The hm1 locus has the highest nucleotide diversity of any gene yet sampled in the wild ancestor of maize, and it contains a large number of indel polymorphisms. There is no evidence, however, that high diversity in hm1 is a product of nonneutral evolution. In contrast, hm2 has very low nucleotide diversity in the wild ancestor of maize. The distribution of hm2 polymorphic sites is consistent with nonneutral evolution, as indicated by Tajima's D and other neutrality tests. In addition, one hm2 haplotype is more frequent than expected under the equilibrium neutral model, suggesting hitchhiking selection. Both defense genes retain >80% of the level of genetic variation in maize relative to the wild ancestor, and this level is similar to other maize genes that were not subject to artificial selection during domestication.     

Geographic variation in adaptation at the molecular level: a case study of plant immunity genes

Natural selection imposed by interacting species frequently varies among geographic locations and can lead to local adaptation, where alternative phenotypes are found in different populations. Little is known, however, about whether geographically variable selection acting on traits that mediate species interactions is consistent or strong enough to influence patterns of nucleotide variation at individual loci. To investigate this question, we examined patterns of nucleotide diversity and population structure at 16 plant innate immunity genes, with putative functions in defending plants against pathogens or herbivores, from six populations of teosinte (Zea mays ssp. parviglumis). Specifically, we tested whether patterns of population structure and within-population diversity at immunity genes differed from patterns found at nonimmunity (reference) loci and from neutral expectations derived from coalescent simulations of structured populations. For the majority of genes, we detected no strong evidence of geographically variable selection. However, in the wound-induced serine protease inhibitor (wip1), which inhibits the hydrolysis of dietary proteins in insect herbivores, one population showed unusually high levels of genetic differentiation, very low levels of nucleotide polymorphism, and was fixed for a novel replacement substitution in the active site of the protein. Taken together, these data suggest that wip1 experienced a recent selective sweep in one geographic region; this pattern may reflect local adaptation or an ongoing species-wide sweep. Overall, our results indicate that a signature of local adaptation at the molecular level may be uncommon-particularly for traits that are under complex genetic control.     

Genetic diversity and the evolutionary history of plant immunity genes in two species of Zea

Plant pathogenesis-related genes (PR genes) code for enzymes, enzyme inhibitors, and other peptides that confer resistance to pathogens and herbivores. Although several PR genes have been the subject of molecular population genetic analyses, a general understanding of their long-term evolutionary dynamics remains incomplete. Here we analyze sequence data from 17 PR genes from two closely related teosinte species of central Mexico. In addition to testing whether patterns of diversity at individual loci depart from expectations under a neutral model, we compared patterns of diversity at defense genes, as a class, to nondefense genes. In Zea diploperennis, the majority of defense genes have patterns of diversity consistent with neutral expectations while at least two genes showed evidence of recent positive selection consistent with arms-race models of antagonistic coevolution. In Zea mays ssp. parviglumis, by contrast, analyses of both defense and nondefense genes revealed strong and consistent departures from the neutral model, suggestive of nonequilibrium population dynamics or population structure. Nevertheless, we found a significant excess of replacement polymorphism in defense genes compared to nondefense genes. Although we cannot exclude relaxed selective constraint as an explanation, our results are consistent with temporally variable (transient or episodic) selection or geographically variable selection acting on parviglumis defense genes. The different patterns of diversity found in the two Zea species may be explained by parviglumis' greater distribution and population structure together with geographic variation in selection.     

Natural History of Innate Host Defense Peptides

Host defense peptides act on the forefront of innate immunity, thus playing a central role in the survival of animals and plants. Despite vast morphological changes in species through evolutionary history, all animals examined to date share common features in their innate immune defense strategies, hereunder expression of host defense peptides (HDPs). Most studies on HDPs have focused on humans, domestic and laboratory animals. More than a thousand different sequences have been identified, yet data on HDPs in wild-living animals are sparse. The biological functions of HDPs include broad-spectrum antimicrobial activity and immunomodulation. Natural selection and coevolutionary host-pathogen arms race theory suggest that the extent and specificity of the microbial load influences the spectrum and potency of HDPs in different species. Individuals of extant species—that have lived for an extended period in evolutionary history amid populations with intact processes of natural selection—likely possess the most powerful and well-adapted “natural antibiotics”. Research on the evolutionary history of the innate defense system and the host in context of the consequences of challenges as well as the efficacy of the innate immune system under natural conditions is therefore of immediate interest. This review focuses on evolutionary aspects of immunophysiology, with emphasis on innate effector molecules. Studies on host defense in wild-living animals may significantly enhance our understanding of inborn immune mechanisms, and help identify molecules that may assist us to cope better with the increasing microbial challenges that likely follow from the continuous amplification of biodiversity levels on Earth.     

Characterization of wound-induced serine protease inhibitor (wip1) genes and proteins in Turkish maize varieties

Protease inhibitors (PIs) are generally small proteins that have been identified in plants. The wip1 gene codes for wound-induced protein, which is similar to serine PIs of the Bowman-Birk family (BBIs). In this study, we analyzed 10 wip1 genes of Turkish maize varieties to understand the structure and characteristics of the wip1 genes and proteins in maize. We found that genetic variability of wip1 genes was higher (π: 0.0173) than reported in previous studies. Tajima’s D value was found to be positive (1.73), suggesting over-dominant selection in these loci. According to phylogenetic analysis of wip1 proteins, monocot and dicot BBIs were separated independently, and Turkish varieties were clustered with each other generally. The 3D structures of wip1 proteins indicated that several wip1 proteins had structural divergence in active loops, containing various numbers of cysteine residues ranging between 7 and 9. Particularly, Cys74 was identified in Kocbey and Gozdem varieties, whereas Cys98 was only in the Gozdem variety. Also, a critical serine residue (Ser98) was observed in two varieties — Antbey and Batem Efe. These results can contribute to understanding the role of wip1 genes and corresponding proteins in maize.     

Comparative evolutionary histories of chitinase genes in the Genus zea and Family poaceae

Patterns of DNA sequence diversity vary widely among genes encoding proteins that protect plants against pathogens and herbivores. Comparative studies may help determine whether these differences are due to the strength of selection acting on different types of defense, in different evolutionary lineages, or both. I analyzed sequence diversity at three chitinases, a well-studied component of defense, in two species of Zea and several Poaceae taxa. Although the Zea species are closely related and these genes code for proteins with similar biochemical function, patterns of diversity vary widely within and among species. Intraspecific diversity at chiB, chiI, and Z. mays ssp. parviglumis chiA are consistent with a neutral-equilibrium model whereas chiA had no segregating sites within Z. diploperennis--consistent with a recent and strong selective sweep. Codons identified as having diverged among Poaceae taxa in response to positive selection were significantly overrepresented among targets of selection in Arabis, suggesting common responses to selection in distantly related plant taxa. Divergence of the recent duplicates chiA and chiB is consistent with positive selection but relaxed constraint cannot be rejected. Weak evidence for adaptive divergence of these duplicated downstream components of defense contrasts with strong evidence for adaptive divergence of genes involved in pathogen recognition.     

Historical Divergence and Gene Flow in the Genus Zea

Gene flow plays a fundamental role in plant evolutionary history, yet its role in population divergence—and ultimately speciation—remains poorly understood. We investigated gene flow and the modalities of divergence in the domesticate Zea mays ssp. mays and three wild Zea taxa using sequence polymorphism data from 26 nuclear loci. We described diversity across loci and assessed evidence for adaptive and purifying selection at nonsynonymous sites. For each of three divergence events in the history of these taxa, we used approximate Bayesian simulation to estimate population sizes and divergence times and explicitly compare among alternative models of divergence. Our estimates of divergence times are surprisingly consistent with previous data from other markers and suggest rapid diversification of lineages within Zea in the last ~150,000 years. We found widespread evidence of historical gene flow, including evidence for divergence in the face of gene flow. We speculate that cultivated maize may serve as a bridge for gene flow among otherwise allopatric wild taxa.     

Species Invasion History Influences Community Evolution in a Tri-Trophic Food Web Model

Background

Recent experimental studies have demonstrated the importance of invasion history for evolutionary formation of community. However, only few theoretical studies on community evolution have focused on such views.

Methodology and Principal Findings

We used a tri-trophic food web model to analyze the coevolutionary effects of ecological invasions by a mutant and by a predator and/or resource species of a native consumer species community and found that ecological invasions can lead to various evolutionary histories. The invasion of a predator makes multiple evolutionary community histories possible, and the evolutionary history followed can determine both the invasion success of the predator into the native community and the fate of the community. A slight difference in the timing of an ecological invasion can lead to a greatly different fate. In addition, even greatly different community histories can converge as a result of environmental changes such as a predator trait shift or a productivity change. Furthermore, the changes to the evolutionary history may be irreversible.

Conclusions and Significance

Our modeling results suggest that the timing of ecological invasion of a species into a focal community can largely change the evolutionary consequences of the community. Our approach based on adaptive dynamics will be a useful tool to understand the effect of invasion history on evolutionary formation of community.     

Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.     

Sequence diversity in the tetraploid Zea perennis and the closely related diploid Z. diploperennis: insights from four nuclear loci

Polyploidy has been an extremely common phenomenon in the evolutionary history of angiosperms. Despite this there are few data available to evaluate the effects of polyploidy on genetic diversity and to compare the relative effects of drift and selection in polyploids and related diploids. We investigated DNA sequence diversity at four nuclear loci (adh1, glb1, c1, and waxy) from the tetraploid Zea perennis and the closely related diploid Z. diploperennis. Contrary to expectations, we detected no strong evidence for greater genetic diversity in the tetraploid, or for consistent differences in the effects of either drift or selection between the tetraploid and the diploid. Our failure to find greater genetic diversity in Z. perennis may result from its relatively recent origin or demographic factors associated with its origin. In addition to comparing genetic diversity in the two species, we constructed genealogies to infer the evolutionary origin of Z. perennis. Although these genealogies are equivocal regarding the mode of origin, several aspects of these genealogies support an autotetraploid origin. Consistent with previous molecular data the genealogies do not, however, support the division of Zea into two sections, the section Zea and the section Luxuriantes.     

Evolution of the TIR domain-containing adaptors in humans: swinging between constraint and adaptation

Natural selection is expected to act strongly on immune system genes as hosts adapt to novel, diverse, and coevolving pathogens. Population genetic studies of host defense genes with parallel functions in model organisms have revealed distinct evolutionary histories among the different components-receptors, adaptors, and effectors-of the innate immune system. In humans, however, detailed evolutionary studies have been mainly confined to the receptors and in particular to Toll-like receptors (TLRs). By virtue of a toll/interleukin-1 receptor (TIR) domain, TLRs activate distinct signaling pathways, which are mediated by the five TIR-containing adaptors: myeloid differentiation factor-88 (MyD88), myeloid differentiation factor-88 adaptor-like protein (MAL), toll/interleukin-1 receptor domain-containing adaptor protein inducing interferon (IFN)β (TRIF), toll/interleukin-1 receptor domain-containing adaptor protein inducing IFNβ-related adaptor molecule (TRAM), and sterile α- and armadillo motif-containing protein (SARM). Here, we have examined the extent to which natural selection has affected immune adaptors in humans, using as a paradigm the TIR-containing adaptors. To do so, we characterized their levels of naturally occurring genetic variation in various human populations. We found that MyD88 and TRIF have mainly evolved under purifying selection, suggesting that their role in the early stages of signal transduction is essential and nonredundant for host survival. In addition, the adaptors have been targeted by multiple episodes of positive selection, differing in timing and spatial location. MyD88 and SARM display signatures of a selective sweep that has occurred in all humans, whereas for the other three adaptors, we detected signatures of adaptive evolution that are restricted to specific populations. Our study provides evidence that the contemporary diversity of the five TIR-containing adaptors results from the intermingling of different selective events, swinging between constraint and adaptation.     

Wip1 phosphatase positively modulates dendritic spine morphology and memory processes through the p38MAPK signaling pathway

Dendritic spine morphology is modulated by protein kinase p38, a mitogen-activated protein (MAPK), in the hippocampus. Protein p38MAPK is a substrate of wip1, a protein phosphatase. The role of wip1 in the central nervous system (CNS) has never been explored. Here, we report a novel function of wip1 in dendritic spine morphology and memory processes. Wip1 deficiency decreases dendritic spine size and density in pyramidal neurons of the hippocampal CA1 region. Simultaneously, impairments in object recognition tasks and contextual memory occur in wip1 deficient mice, but are reversed in wip1/p38 double mutant mice. Thus, our findings demonstrate that wip1 modulates dendritic morphology and memory processes through the p38MAPK signaling pathway. In addition to the well-characterized role of the wip1/p38MAPK in cell death and differentiation, we revealed the novel contribution of wip1 to cognition and dendritic spine morphology, which may suggest new approaches to treating neurodegenerative disorders.     

Wip1 phosphatase positively modulates dendritic spine morphology and memory processes through the p38MAPK signaling pathway

Dendritic spine morphology is modulated by protein kinase p38, a mitogen-activated protein (MAPK), in the hippocampus. Protein p38MAPK is a substrate of wip1, a protein phosphatase. The role of wip1 in the central nervous system (CNS) has never been explored. Here, we report a novel function of wip1 in dendritic spine morphology and memory processes. Wip1 deficiency decreases dendritic spine size and density in pyramidal neurons of the hippocampal CA1 region. Simultaneously, impairments in object recognition tasks and contextual memory occur in wip1 deficient mice, but are reversed in wip1/p38 double mutant mice. Thus, our findings demonstrate that wip1 modulates dendritic morphology and memory processes through the p38MAPK signaling pathway. In addition to the well-characterized role of the wip1/p38MAPK in cell death and differentiation, we revealed the novel contribution of wip1 to cognition and dendritic spine morphology, which may suggest new approaches to treating neurodegenerative disorders.     

Evolutionary patterns in the sequence and structure of transfer RNA: a window into early translation and the genetic code

Transfer RNA (tRNA) molecules play vital roles during protein synthesis. Their acceptor arms are aminoacylated with specific amino acid residues while their anticodons delimit codon specificity. The history of these two functions has been generally linked in evolutionary studies of the genetic code. However, these functions could have been differentially recruited as evolutionary signatures were left embedded in tRNA molecules. Here we built phylogenies derived from the sequence and structure of tRNA, we forced taxa into monophyletic groups using constraint analyses, tested competing evolutionary hypotheses, and generated timelines of amino acid charging and codon discovery. Charging of Sec, Tyr, Ser and Leu appeared ancient, while specificities related to Asn, Met, and Arg were derived. The timelines also uncovered an early role of the second and then first codon bases, identified codons for Ala and Pro as the most ancient, and revealed important evolutionary take-overs related to the loss of the long variable arm in tRNA. The lack of correlation between ancestries of amino acid charging and encoding indicated that the separate discoveries of these functions reflected independent histories of recruitment. These histories were probably curbed by co-options and important take-overs during early diversification of the living world.     

Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis

Recent studies of allocation to defensive chemicals in plants have provided insights into the ecological controls over plant defensive chemicals. Both developmental and ecological studies now suggest that we can understand the factors influencing allocation to defense by examining the relative availability of resources, external needs for chemical defense, and the internal demands for growth that plants face. These studies have also shed light on one of the more popular theories in plant evolutionary ecology, the growth-differentiation balance hypothesis of plant resource allocation.     

A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry

Many facets of plant form and function are reflected in general cross‐taxa scaling relationships. Metabolic scaling theory (MST) and the leaf economics spectrum (LES) have each proposed unifying frameworks and organisational principles to understand the origin of botanical diversity. Here, we test the evolutionary assumptions of MST and the LES using a cross of two genetic variants of Arabidopsis thaliana. We show that there is enough genetic variation to generate a large fraction of variation in the LES and MST scaling functions. The progeny sharing the parental, naturally occurring, allelic combinations at two pleiotropic genes exhibited the theorised optimum ¾ allometric scaling of growth rate and intermediate leaf economics. Our findings: (1) imply that a few pleiotropic genes underlie many plant functional traits and life histories; (2) unify MST and LES within a common genetic framework and (3) suggest that observed intermediate size and longevity in natural populations originate from stabilising selection to optimise physiological trade‐offs.     

An evolutionary perspective on leaf economics: phylogenetics of leaf mass per area in vascular plants

In plant leaves, resource use follows a trade‐off between rapid resource capture and conservative storage. This “worldwide leaf economics spectrum” consists of a suite of intercorrelated leaf traits, among which leaf mass per area, LMA, is one of the most fundamental as it indicates the cost of leaf construction and light‐interception borne by plants. We conducted a broad‐scale analysis of the evolutionary history of LMA across a large dataset of 5401 vascular plant species. The phylogenetic signal in LMA displayed low but significant conservatism, that is, leaf economics tended to be more similar among close relatives than expected by chance alone. Models of trait evolution indicated that LMA evolved under weak stabilizing selection. Moreover, results suggest that different optimal phenotypes evolved among large clades within which extremes tended to be selected against. Conservatism in LMA was strongly related to growth form, as were selection intensity and phenotypic evolutionary rates: woody plants showed higher conservatism in relation to stronger stabilizing selection and lower evolutionary rates compared to herbaceous taxa. The evolutionary history of LMA thus paints different evolutionary trajectories of vascular plant species across clades, revealing the coordination of leaf trait evolution with growth forms in response to varying selection regimes.     

Phylogenetic and expression analysis of ZnF-AN1 genes in plants

In plants, ZnF-AN1 genes are part of a multigene family with 13 members in Arabidopsis thaliana, 19 members in Populus trichocarpa, 17 members in Oryza sativa, at least 11 members in Zea mays, and 2 members in Chlamydomonas reinhardtii. All ZnF-AN1 genes contain the ZnF-AN1 domain. According to the phylogenetic analysis of the ZnF-AN1 domain, we divided plant ZnF-AN1 genes into two types. The coding sequences of most type I members do not possess any introns, while most type II members do possess intron(s). Through Northern blot analysis of maize members and digital Northern analysis of Arabidopsis members, we found that most ZnF-AN1 genes are involved in responses to abiotic stresses. The evolutionary analysis indicated that the expansion rate of type I was higher than that of type II. After expansion, some ZnF-AN1 genes may have gained new functions, some may have lost their functions, and some were specialized to perform their functions in stress-specific or tissue-specific modes. In addition, we propose an evolutionary model of type II ZnF-AN1 genes in plants.