Metabolomics analysis reveals differences in evolution between maize and rice

Metabolites are the intermediate and final products of metabolism, which play essential roles in plant growth, evolution and adaptation to changing climates. However, it is unclear how evolution contributes to metabolic variation in plants. Here, we investigated the metabolomics data from leaf and seed tissues in maize and rice. Using principal components analysis based on leaf metabolites but not seed metabolites, metabolomics data could be clearly separated for rice Indica and Japonica accessions, while two maize subgroups, temperate and tropical, showed more visible admixture. Rice and maize seed exhibited significant interspecific differences in metabolic variation, while within rice, leaf and seed displayed similar metabolic variations. Among 10 metabolic categories, flavonoids had higher variation in maize than rice, indicating flavonoids are a key constituent of interspecific metabolic divergence. Interestingly, metabolic regulation was also found to be reshaped dramatically from positive to negative correlations, indicative of the differential evolutionary processes in maize and rice. Moreover, perhaps due to this divergence significantly more metabolic interactions were identified in rice than maize. Furthermore, in rice, the leaf was found to harbor much more intense metabolic interactions than the seed. Our result suggests that metabolomes are valuable for tracking evolutionary history, thereby complementing and extending genomic insights concerning which features are responsible for interspecific differentiation in maize and rice.     

The evolution of apomixis in angiosperms: A reappraisal

Abstract

Apomixis, the asexual reproduction via seed, has long been regarded a blind alley of evolution. This hypothesis was based on the assumption that apomixis is an irreversible, phylogenetically derived trait that would rapidly lead to extinction of the respective lineages. However, recent updates of the taxonomic distribution of apomixis in angiosperms suggest an alternative evolutionary scenario. Apomixis is taxonomically scattered and occurs in both early and late branching lineages, with several reversals from apomixis to obligate sex along phylogeny. Genetic control of apomixis is based on altered expression patterns of the same genes that control sexual development; epigenetic changes following polyploidization and/or hybridization may trigger shifts from sexuality to apomixis. Mendelian inheritance confirms the facultative nature and possible reversibility of apomixis to sexual reproduction. Apomixis, therefore, could represent a transition period in the evolution of polyploid complexes, with polyspory in paleopolyploids being a remnant of lost apomixis. In neopolyploids, apomixis helps to overcome sterility and allows for geographical range expansions of agamic polyploid complexes. The facultative nature of apomixis allows for reversal to sexuality and further speciation of paleopolyploid lineages. Thus, apomixis may facilitate diversification of polyploid complexes and evolution in angiosperms.     

The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention

Stamens that have lost their primary function of pollen production, or staminodes, occur uncommonly within angiosperms, but frequently fulfill important secondary floral functions. The phylogenetic distribution of staminodes suggests that they typically arise during evolutionary reduction of the androecium. Differences in the genetic control and patterns of stamen loss between actinomorphic and zygomorphic flowers shape staminode development. In clades with actinomorphic flowers, staminodes generally replace an entire stamen whorl and staminode loss seems irreversible. In contrast, in clades with zygomorphic flowers staminodes evolve from a subset of the stamens in a whorl and staminodes can reappear in a lineage after being lost (e.g., Cheloneae, Scrophulariaceae). If staminodes do not adopt new functions during androecium reduction they are lost quickly, so that nonfunctional staminodes appear only in recently derived taxa. Alternatively, when staminodes assume new floral roles, either directly or indirectly after a nonfunctional period, they can become integral floral components which perpetuate within clades (e.g., Orchidaceae). Indirect evolution of staminode function allows greater flexibility of function by allowing staminodes to take over roles not performed by stamens, such as involvement in mechanisms to prevent self-pollination and mechanisms of explosive pollination. Multifunctional staminodes characterize lineages with universal or widespread staminodes.     

Temperatures and the growth and development of maize and rice: a review

Because of global land surface warming, extreme temperature events are expected to occur more often and more intensely, affecting the growth and development of the major cereal crops in several ways, thus affecting the production component of food security. In this study, we have identified rice and maize crop responses to temperature in different, but consistent, phenological phases and development stages. A literature review and data compilation of around 140 scientific articles have determined the key temperature thresholds and response to extreme temperature effects for rice and maize, complementing an earlier study on wheat. Lethal temperatures and cardinal temperatures, together with error estimates, have been identified for phenological phases and development stages. Following the methodology of previous work, we have collected and statistically analysed temperature thresholds of the three crops for the key physiological processes such as leaf initiation, shoot growth and root growth and for the most susceptible phenological phases such as sowing to emergence, anthesis and grain filling. Our summary shows that cardinal temperatures are conservative between studies and are seemingly well defined in all three crops. Anthesis and ripening are the most sensitive temperature stages in rice as well as in wheat and maize. We call for further experimental studies of the effects of transgressing threshold temperatures so such responses can be included into crop impact and adaptation models.     

Diversity and distribution of Burkholderia cepacia complex in the rhizosphere of rice and maize

A survey of Burkholderia cepacia complex (Bcc) species was conducted in agricultural fields within Hangzhou, China. Out of the 251 bacterial isolates recovered on the selective media from the rhizosphere of rice and maize, 112 of them were assigned to Bcc by PCR assays. The species composition of the Bcc isolates was analyzed by a combination of recA-restriction fragment length polymorphism assays, species-specific PCR tests and recA gene sequencing. The results revealed that the majority belong to B. cepacia, Burkholderia cenocepacia recA lineage IIIB, Burkholderia vietnamiensis and Burkholderia pyrrocinia. Burkholderia cenocepacia and B. vietnamiensis dominated the rhizosphere of maize and rice, respectively, indicating that species composition and abundance of Bcc may vary dramatically in different crop rhizospheres. In addition, one isolate (R456) formed a single discrete cluster within the phylogenetic analysis of the Bcc recA gene, and it may belong to a new genomovar.     

The promoter of rbcS in a C3 plant (rice) directs organ-specific,light-dependent expression in a C4 plant (maize), but does not confer bundle sheath cell-specific expression

The small subunit of ribulose-bisphosphate carboxylase (Rubisco), encoded by rbcS, is essential for photosynthesis in both C3 and C4 plants, even though the cell specificity of rbcS expression is different between C3 and C4 plants. The C3 rbcS is specifically expressed in mesophyll cells, while the C4 rbcS is expressed in bundle sheath cells, and not mesophyll cells. Two chimeric genes were constructed consisting of the structural gene encoding -glucuronidase (GUS) controlled by the two promoters from maize (C4) and rice (C3) rbcS genes. These constructs were introduced into a C4 plant, maize. Both chimeric genes were specifically expressed in photosynthetic organs, such as leaf blade, but not in non-photosynthetic organs. The expressions of the genes were also regulated by light. However, the rice promoter drove the GUS activity mainly in mesophyll cells and relatively low in bundle sheath cells, while the maize rbcS promoter induced the activity specifically in bundle sheath cells. These results suggest that the rice promoter contains some cis-acting elements responding in an organ-pecific and light-inducible regulation manner in maize but does not contain element(s) for bundle sheath cell-specific expression, while the maize promoter does contain such element(s). Based on this result, we discuss the similarities and differences between the rice (C3) and maize (C4) rbcS promoter in terms of the evolution of the C4 photosynthetic gene.     

Gravitropism of maize and rice coleoptiles: dependence on the stimulation angle

Gravitropism of maize and rice coleoptiles was investigated with respect to its dependence on the angle of displacement or the initial stimulation angle (ISA). Close examination of curvature kinetics and the response to a drop in stimulation angle (SA) indicated that the gravtropic response during an early but substantial part of the curvature development is directly related to the ISA, there being no effect of the reduction of SA resulting from the curvature response itself. On the basis of this finding, the relationship between the steady SA and the curvature rate was determined. In maize, the curvature rate increased linearly with the sines of SAs up to an SA of 90 degrees. Rice coleoptiles, however, showed a saturation curve in the same range of SAs. The saturation profile was nearly identical between coleoptiles grown in air and those submerged in water, although the latter elongated much faster. Rice coleoptiles appeared to be far more sensitive to gravity than maize coleoptiles. It is concluded that the sensitivity to gravity, assessed through dependence on ISA, is a property inherent to a given gravitropic organ. Long-term measurements of curvature indicated that the coleoptiles bend back past the vertical. This overshooting was marked in submerged rice coleoptiles.     

The turbulent life of Sirevirus retrotransposons and the evolution of the maize genome: more than ten thousand elements tell the story

Sireviruses are one of the three genera of Copia long terminal repeat (LTR) retrotransposons, exclusive to and highly abundant in plants, and with a unique, among retrotransposons, genome structure. Yet, perhaps due to the few references to the Sirevirus origin of some families, compounded by the difficulty in correctly assigning retrotransposon families into genera, Sireviruses have hardly featured in recent research. As a result, analysis at this key level of classification and details of their colonization and impact on plant genomes are currently lacking. Recently, however, it became possible to accurately assign elements from diverse families to this genus in one step, based on highly conserved sequence motifs. Hence, Sirevirus dynamics in the relatively obese maize genome can now be comprehensively studied. Overall, we identified >10 600 intact and approximately 28 000 degenerate Sirevirus elements from a plethora of families, some brought into the genus for the first time. Sireviruses make up approximately 90% of the Copia population and it is the only genus that has successfully infiltrated the genome, possibly by experiencing intense amplification during the last 600 000 years, while being constantly recycled by host mechanisms. They accumulate in chromosome-distal gene-rich areas, where they insert in between gene islands, mainly in preferred zones within their own genomes. Sirevirus LTRs are heavily methylated, while there is evidence for a palindromic consensus target sequence. This work brings Sireviruses in the spotlight, elucidating their lifestyle and history, and suggesting their crucial role in the current genomic make-up of maize, and possibly other plant hosts.     

Immunogold labelling of xylans and arabinoxylans in the plant cell walls of maize stem

Summary— Polyclonal antibodies against 4-O-methyl-glucuronoxylan and α L-1-3 arabinofuranosyl poly-β-d-1-4-xylopyranosyl were raised from rabbits. An immunocytochemical technique was used to localize xylans and arabinoxylans in the plant cell walls of the apical internode of two maize lines of different digestibility. The sclerenchyma, fibres and xylem (lignified tissues) and the parenchyma (non-lignified tissue) were studied. The arabinoxylans were more heavily labelled than the xylans in the lignified tissues of the less digestible maize whereas in the more digestible line the labelling of the two polysaccharides was similar. The xylans and arabinoxylans were localized in the secondary cell wall. In both maize lines, labelling increased from the base upwards of the apical internode, reflecting the changes in growth stage.     

Expression of the maize proteinase inhibitor (mpi) gene in rice plants enhances resistance against the striped stem borer (Chilo suppressalis): effects on larval growth and insect gut proteinases

The maize proteinase inhibitor (mpi) gene was introduced into two elite japonica rice varieties. Both constitutive expression of the mpi gene driven by the maize ubiquitin 1 promoter and wound-inducible expression of the mpi gene driven by its own promoter resulted in the accumulation of MPI protein in the transgenic plants. No effect on plant phenotype was observed in mpi-expressing lines. The stability of transgene expression through successive generations of mpi rice lines (up to the T(4) generation) and the production of functional MPI protein were confirmed. Expression of the mpi gene in rice enhanced resistance to the striped stem borer (Chilo suppressalis), one of the most important pests of rice. In addition, transgenic mpi plants were evaluated in terms of their effects on the growth of C. suppressalis larvae and the insect digestive proteolytic system. An important dose-dependent reduction of larval weight of C. suppressalis larvae fed on mpi rice, compared with larvae fed on untransformed rice plants, was observed. Analysis of the digestive proteolytic activity from the gut of C. suppressalis demonstrated that larvae adapted to mpi transgene expression by increasing the complement of digestive proteolytic activity: the serine and cysteine endoproteinases as well as the exopeptidases leucine aminopeptidase and carboxypeptidases A and B. However, the induction of such proteolytic activity did not prevent the deleterious effects of MPI on larval growth. The introduction of the mpi gene into rice plants can thus be considered as a promising strategy to protect rice plants against striped stem borer.     

The skull evolution of oviraptorosaurian dinosaurs: the role of niche partitioning in diversification

Oviraptorosaurs are bird‐like theropod dinosaurs that thrived in the final pre‐extinction ecosystems during the latest Cretaceous, and the beaked, toothless skulls of derived species are regarded as some of the most peculiar among dinosaurs. Their aberrant morphologies are hypothesized to have been caused by rapid evolution triggered by an ecological/biological driver, but little is known about how their skull shapes and functional abilities diversified. Here, we use quantitative techniques to study oviraptorosaur skull form and mandibular function. We demonstrate that the snout is particularly variable, that mandibular form and upper/lower beak form are significantly correlated with phylogeny, and that there is a strong and significant correlation between mandibular function and mandible/lower beak shape, suggesting a form–function association. The form–function relationship and phylogenetic signals, along with a moderate allometric signal in lower beak form, indicate that similar mechanisms governed beak shape in oviraptorosaurs and extant birds. The two derived oviraptorosaur clades, oviraptorids and caenagnathids, are significantly separated in morphospace and functional space, indicating that they partitioned niches. Oviraptorids coexisting in the same ecosystem are also widely spread in morphological and functional space, suggesting that they finely partitioned feeding niches, whereas caenagnathids exhibit extreme disparity in beak size. The diversity of skull form and function was likely key to the diversification and evolutionary success of oviraptorosaurs in the latest Cretaceous.     

The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution

Investigations into the evolution of the primate brain have tended to neglect the role of connectivity in determining which brain structures have changed in size, focusing instead on changes in the size of the whole brain or of individual brain structures, such as the neocortex, in isolation. We show that the primate cerebellum, neocortex, vestibular nuclei and relays between them exhibit correlated volumetric evolution, even after removing the effects of change in other structures. The patterns of correlated evolution among individual nuclei correspond to their known patterns of connectivity. These results support the idea that the brain evolved by mosaic size change in arrays of functionally connected structures. Furthermore, they suggest that the much discussed expansion of the primate neocortex should be re-evaluated in the light of conjoint cerebellar expansion.     

Climatic niche evolution in Smilacaceae (Liliales) drives patterns of species diversification and richness between the Old and New World

Geographical variation in species richness in plant groups is determined by the interplay between historical, evolutionary, and ecological processes. However, the processes underlying the striking disparity in species richness between Asia and the Americas remain poorly understood. Here, we synthesize global phylogenetic and macroecological data on the diversification of Smilacaceae, deciphering potential drivers underlying the species diversity pattern biased toward Asia. We compiled global distributions of all Smilacaceae species, and reconstructed the biogeographic history and niche evolution using a new time-calibrated phylogeny (eight genes, 135 species). Integrating these data sets, we estimated evolutionary histories and diversification rates for each region, and tested correlations among species diversification, niche evolution, and niche divergence. Smilacaceae probably originated during the Late Cretaceous/Early Palaeocene and began to diversify in middle to low latitudes in Central America and Eurasia during the Late Eocene. Both the Old and New World clades exhibited a steady, albeit slight, increase of species diversification from the Late Eocene to Early Miocene. However, the Old World clade experienced an abrupt increase in net diversification during the Late Miocene. Our findings also revealed that species diversification rates were positively correlated with ecological niche evolution and niche divergence. Niche shifts and climatic niche evolution since the Middle Miocene played crucial roles in species diversification dynamics within Smilacaceae. The high plant richness in Asia may be explained by greater diversification in this region, potentially promoted by heterogeneous environments.     

Effects of culture media on hCTLA4Ig production and protein expression patterns in transgenic rice cell suspension cultures

The effects of culture media on the production of human cytotoxic T-lymphocyte antigen 4-immunoglobulin (hCTLA4Ig) and intracellular protein expression patterns were investigated in transgenic rice cell suspension cultures. Using comparative proteomic analysis, changes in the intracellular proteome in different culture media were identified. Culture media were found to be an important factor for the production of the recombinant target protein in this expression system, which was under the control of the rice α-amylase 3D (RAmy3D) promoter. In terms of hCTLA4Ig production, the N6 medium produced a 3.7-fold higher level of protein than the AA medium. In addition, the N6 medium provided better protein stability and cell viability. In the intracellular proteome analysis, we identified eight proteomes that were differentially expressed. These results could provide valuable information for the improvement of cell growth and target protein production.     

Demographic constraints in evolution: Towards unifying the evolutionary theories of senescence and niche conservatism

Summary I suggest that there may be a fundamental conceptual unity between two seemingly disparate phenomena: (1) senescence (the progressive deterioration in physiological function and, thus, individual fitness with age) and (2) niche conservatism (the observation that species often seem rather fixed over evolutionary time in their basic niche properties). I argue that both phenomena arise from demographic asymmetries. The evolutionary theory of ageing rests on the observation that the force of selection declines with age, reflecting the basic demographic facts that in persistent populations there are always fewer individuals in old than in young age classes and these individuals tend to have lower reproductive value. A similar demographic asymmetry arises when populations inhabit environments with source habitats (i.e. where conditions are within the species' niche) and sink habitats (where conditions lie outside the niche): there tend to be more individuals in sources than in sinks and individuals in sources have relatively higher reproductive values. These demographic asymmetries should often imply that the force of selection is greater in sources than in sinks, leading automatically towards niche conservatism. I suggest that niche evolution is most likely in circumstances where these demographic asymmetries in space weaken or reverse.     

Behavioural environments and niche construction: the evolution of dim-light foraging in bees

Most bees forage for floral resources during the day, but temporal patterns of foraging activity vary extensively, and foraging in dim-light environments has evolved repeatedly. Facultative dim-light foraging behaviour is known in five of nine families of bees, while obligate behaviour is known in four families and evolved independently at least 19 times. The light intensity under which bees forage varies by a factor of 10⁸, and therefore the evolution of dim-light foraging represents the invasion of a new, extreme niche. The repeated evolution of dim-light foraging behaviour in bees allows tests of the hypothesis that behaviour acts as an evolutionary pacemaker. With the exception of one species of Apis , facultative dim-light foragers show no external structural traits that are thought to enable visually mediated flight behaviour in low-light environments. By contrast, most obligate dim-light foragers show a suite of convergent optical traits such as enlarged ocelli and compound eyes. In one intensively studied species ( Megalopta genalis ) these optical changes are associated with neurobiological changes to enhance photon capture. The available ecological evidence suggests that an escape from competition for pollen and nectar resources and avoidance of natural enemies are driving factors in the evolution of obligate dim-light foraging.