Maria S. Vorontsova

Anatomical enablers and the evolution of C4 photosynthesis in grasses

C4 photosynthesis is a series of anatomical and biochemical modifications to the typical C3 pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C4 origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C4 evolvability in certain phylogenetic groups. The C4 trait has evolved 22–24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C3 taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C4 evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C4 evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C4 origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C3 context and preceding the emergence of the C4 syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.

Wild Relatives of the Eggplant (Solanum melongena L.: Solanaceae): New Understanding of Species Names in a Complex Group

Background The common or brinjal eggplant (Solanum melongena L.) belongs to the Leptostemonum Clade (the “spiny” solanums) of the species-rich genus Solanum (Solanaceae). Unlike most of the genus, the eggplant and its relatives are from the Old World; most eggplant wild relatives are from Africa. An informal system for naming eggplant wild relatives largely based on crossing and other biosystematics data has been in use for approximately a decade. This system recognises several forms of two broadly conceived species, S. incanum L. and S. melongena. Recent morphological and molecular work has shown that species-level differences exist between these entities, and a new species-level nomenclature has been identified as necessary for plant breeders and for the maintenance of accurately named germplasm. Methodology/Principal Findings We examined herbarium specimens from throughout the wild species ranges as part of a larger revision of the spiny solanums of Africa. Based on these morphological and molecular studies, we delimited species in the group to which the common eggplant belongs and constructed identification keys for the group. We also examined the monophyly of the group considered as the eggplant relatives by previous authors. Conclusions/Significance We recognise ten species in this group: S. aureitomentosum Bitter, S. campylacanthum A.Rich., S. cerasiferum Dunal, S. incanum L., S. insanum L., S. lichtensteinii Willd., S. linnaeanum Hepper & P.-M.L.Jaeger, S. melongena L., S. rigidum Lam. and S. umtuma Voronts. & S.Knapp. We review the history of naming and provide keys and character lists for all species. Ploidy level differences have not been investigated in the eggplant wild relatives; we identify this as a priority for improvement of crop wild relative use in breeding. The application of species-level names to these entities will help focus new collecting efforts for brinjal eggplant improvement and help facilitate information exchange.

From museums to genomics: old herbarium specimens shed light on a C3 to C4 transition

Collections of specimens held by natural history museums are invaluable material for biodiversity inventory and evolutionary studies, with specimens accumulated over 300 years readily available for sampling. Unfortunately, most museum specimens yield low-quality DNA. Recent advances in sequencing technologies, so called next-generation sequencing, are revolutionizing phylogenetic investigations at a deep level. Here, the Illumina technology (HiSeq) was used on herbarium specimens of Sartidia (subfamily Aristidoideae, Poaceae), a small African-Malagasy grass lineage (six species) characteristic of wooded savannas, which is the C3 sister group of Stipagrostis, an important C4 genus from Africa and SW Asia. Complete chloroplast and nuclear ribosomal sequences were assembled for two Sartidia species, one of which (S. perrieri) is only known from a single specimen collected in Madagascar 100 years ago. Partial sequences of a few single-copy genes encoding phosphoenolpyruvate carboxylases (ppc) and malic enzymes (nadpme) were also assembled. Based on these data, the phylogenetic position of Malagasy Sartidia in the subfamily Aristidoideae was investigated and the biogeographical history of this genus was analysed with full species sampling. The evolutionary history of two genes for C4 photosynthesis (ppc-aL1b and nadpme-IV) in the group was also investigated. The gene encoding the C4 phosphoenolpyruvate caroxylase of Stipagrostis is absent from S. dewinteri suggesting that it is not essential in C3 members of the group, which might have favoured its recruitment into a new metabolic pathway. Altogether, the inclusion of historical museum specimens in phylogenomic analyses of biodiversity opens new avenues for evolutionary studies.

A global database of C4 photosynthesis in grasses

C3, C4 or Crassulacean acid metabolism (CAM) photosynthetic pathways represent a fundamental axis of trait variation in plants, with importance at scales from genome to biome. Knowing the distribution of these pathways among wild species is a crucial first step in understanding the patterns and processes of photosynthetic evolution and its role in ecological processes at large scales (e.g. changes in the composition of biomes under global change). C4 photosynthesis is most prevalent in the Poaceae (grasses), which account for about half of allC4 species (Sage et al., 1999a).Research on the evolution and ecology of these plants has undergone a renaissance during the last 7 yr, catalyzed by phylogenetic analyses showing multiple parallel C4 origins (e.g. Christin et al., 2007; Vicentini et al., 2008; GPWG II, 2012), insights into the distribution of C4 species and assembly of the C4 grassland biome (Edwards & Still, 2008; Edwards & Smith, 2010; Edwards et al., 2010), and efforts to introduce the C4 pathway into rice (Hibberd et al., 2008; von Caemmerer et al., 2012). C4 photosynthesis is an excellent model for investigating complex trait evolution, because of the broad knowledge base describing its biochemical basis, evolutionary history, and ecological interactions (Christin et al., 2010).

Phylogenomics and taxonomy of Lecomtelleae (Poaceae), an isolated panicoid lineage from Madagascar

BACKGROUND AND AIMS An accurate characterization of biodiversity requires analyses of DNA sequences in addition to classical morphological descriptions. New methods based on high-throughput sequencing may allow investigation of specimens with a large set of genetic markers to infer their evolutionary history. In the grass family, the phylogenetic position of the monotypic genus Lecomtella, a rare bamboo-like endemic from Madagascar, has never been appropriately evaluated. Until now its taxonomic treatment has remained controversial, indicating the need for re-evaluation based on a combination of molecular and morphological data. METHODS The phylogenetic position of Lecomtella in Poaceae was evaluated based on sequences from the nuclear and plastid genomes generated by next-generation sequencing (NGS). In addition, a detailed morphological description of L. madagascariensis was produced, and its distribution and habit were investigated in order to assess its conservation status. KEY RESULTS The complete plastid sequence, a ribosomal DNA unit and fragments of low-copy nuclear genes (phyB and ppc) were obtained. All phylogenetic analyses place Lecomtella as an isolated member of the core panicoids, which last shared a common ancestor with other species >20 million years ago. Although Lecomtella exhibits morphological characters typical of Panicoideae, an unusual combination of traits supports its treatment as a separate group. CONCLUSIONS The study showed that NGS can be used to generate abundant phylogenetic information rapidly, opening new avenues for grass phylogenetics. These data clearly showed that Lecomtella forms an isolated lineage, which, in combination with its morphological peculiarities, justifies its treatment as a separate tribe: Lecomtelleae. New descriptions of the tribe, genus and species are presented with a typification, a distribution map and an IUCN conservation assessment.

Photosynthetic innovation broadens the niche within a single species.

Adaptation to changing environments often requires novel traits, but how such traits directly affect the ecological niche remains poorly understood. Multiple plant lineages have evolved C4 photosynthesis, a combination of anatomical and biochemical novelties predicted to increase productivity in warm and arid conditions. Here, we infer the dispersal history across geographical and environmental space in the only known species with both C4 and non-C4 genotypes, the grass Alloteropsis semialata. While non-C4 individuals remained confined to a limited geographic area and restricted ecological conditions, C4 individuals dispersed across three continents and into an expanded range of environments, encompassing the ancestral one. This first intraspecific investigation of C4 evolutionary ecology shows that, in otherwise similar plants, C4 photosynthesis does not shift the ecological niche, but broadens it, allowing dispersal into diverse conditions and over long distances. Over macroevolutionary timescales, this immediate effect can be blurred by subsequent specialisation towards more extreme niches.

Madagascar's grasses and grasslands: anthropogenic or natural?

Grasses, by their high productivity even under very low pCO2, their ability to survive repeated burning and to tolerate long dry seasons, have transformed the terrestrial biomes in the Neogene and Quaternary. The expansion of grasslands at the cost of biodiverse forest biomes in Madagascar is often postulated as a consequence of the Holocene settlement of the island by humans. However, we show that the Malagasy grass flora has many indications of being ancient with a long local evolutionary history, much predating the Holocene arrival of humans. First, the level of endemism in the Madagascar grass flora is well above the global average for large islands. Second, a survey of many of the more diverse areas indicates that there is a very high spatial and ecological turnover in the grass flora, indicating a high degree of niche specialization. We also find some evidence that there are both recently disturbed and natural stable grasslands: phylogenetic community assembly indicates that recently severely disturbed grasslands are phylogenetically clustered, whereas more undisturbed grasslands tend to be phylogenetically more evenly distributed. From this evidence, it is likely that grass communities existed in Madagascar long before human arrival and so were determined by climate, natural grazing and other natural factors. Humans introduced zebu cattle farming and increased fire frequency, and may have triggered an expansion of the grasslands. Grasses probably played the same role in the modification of the Malagasy environments as elsewhere in the tropics.

Molecular phylogenetics of tribe Poranthereae (Phyllanthaceae; Euphorbiaceae sensu lato)

Novel insights into the evolutionary history of a taxonomically complex tropical plant group were gained in this study using DNA sequence data. A molecular phylogenetic analysis of the newly circumscribed and expanded tribe Poranthereae (Phyllanthaceae) is presented. Sampling included 97 accessions for 63 of c. 120 species. Largely congruent results have been obtained from nuclear ribosomal ITS and plastid matK sequences. These analyses support the recognition of Andrachne and Leptopus as distinct genera. The deceptively similar Andrachne section Phyllanthopsis, Andrachne ovalis, and Leptopus decaisnei are separate lineages to be segregated. Zimmermannia and Zimmermanniopsis are embedded in Meineckia; Oreoporanthera is embedded in Poranthera; and Archileptopus is embedded in Leptopus. Andrachne section Pseudophyllanthus is polyphyletic, the two Madagascan endemics emerging as a sister clade to Meineckia. The noncontiguous distributions of Andrachne sensu lato and Leptopus sensu lato were found to be the result of separate evolutionary histories of morphologically similar clades, whereas Andrachne sensu stricto and Meineckia remain geographically disjunct. Actephila and Leptopus are sisters with a sympatric distribution in humid Asia. Presence of petals appears to be plesiomorphic for the tribe. Petals are reduced in Actephila and Oreoporanthera and lost in the Meineckia clade.

Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait

Physiological novelties are often studied at macro‐evolutionary scales such that their micro‐evolutionary origins remain poorly understood. Here, we test the hypothesis that key components of a complex trait can evolve in isolation and later be combined by gene flow. We use C4 photosynthesis as a study system, a derived physiology that increases plant productivity in warm, dry conditions. The grass Alloteropsis semialata includes C4 and non‐C4 genotypes, with some populations using laterally acquired C4‐adaptive loci, providing an outstanding system to track the spread of novel adaptive mutations. Using genome data from C4 and non‐C4 A. semialata individuals spanning the species’ range, we infer and date past migrations of different parts of the genome. Our results show that photosynthetic types initially diverged in isolated populations, where key C4 components were acquired. However, rare but recurrent subsequent gene flow allowed the spread of adaptive loci across genetic pools. Indeed, laterally acquired genes for key C4 functions were rapidly passed between populations with otherwise distinct genomic backgrounds. Thus, our intraspecific study of C4‐related genomic variation indicates that components of adaptive traits can evolve separately and later be combined through secondary gene flow, leading to the assembly and optimization of evolutionary innovations.

The global distribution of bamboos: assessing correlates of introduction and invasion

Bamboos are one of the most economically important plant groups globally, but this world-wide trade creates risks of invasions. Here we identified 1662 species of bamboo, of which almost a seventh (232) have been introduced outside their native range, with Asiatic and larger species preferred. Only 12 species were found to have become invasive. However, invasiveness was found to be more a function of human-usage than specific species traits, suggesting the recent upsurge in bamboo cultivation could pose future invasion risks.