Mónica Arakaki

Contemporaneous and recent radiations of the world's major succulent plant lineages.

The cacti are one of the most celebrated radiations of succulent plants. There has been much speculation about their age, but progress in dating cactus origins has been hindered by the lack of fossil data for cacti or their close relatives. Using a hybrid phylogenomic approach, we estimated that the cactus lineage diverged from its closest relatives ≈35 million years ago (Ma). However, major diversification events in cacti were more recent, with most species-rich clades originating in the late Miocene, ≈10–5 Ma. Diversification rates of several cactus lineages rival other estimates of extremely rapid speciation in plants. Major cactus radiations were contemporaneous with those of South African ice plants and North American agaves, revealing a simultaneous diversification of several of the worlds major succulent plant lineages across multiple continents. This short geological time period also harbored the majority of origins of C4 photosynthesis and the global rise of C4 grasslands. A global expansion of arid environments during this time could have provided new ecological opportunity for both succulent and C4 plant syndromes. Alternatively, recent work has identified a substantial decline in atmospheric CO2 ≈15–8 Ma, which would have strongly favored C4 evolution and expansion of C4-dominated grasslands. Lowered atmospheric CO2 would also substantially exacerbate plant water stress in marginally arid environments, providing preadapted succulent plants with a sharp advantage in a broader set of ecological conditions and promoting their rapid diversification across the landscape.

C4 eudicots are not younger than C4 monocots

C(4) photosynthesis is a plant adaptation to high levels of photorespiration. Physiological models predict that atmospheric CO(2) concentration selected for C(4) grasses only after it dropped below a critical threshold during the Oligocene (∼30 Ma), a hypothesis supported by phylogenetic and molecular dating analyses. However the same models predict that CO(2) should have reached much lower levels before selecting for C(4) eudicots, making C(4) eudicots younger than C(4) grasses. In this study, different phylogenetic datasets were combined in order to conduct the first comparative analysis of the age of C(4) origins in eudicots. Our results suggested that all lineages of C(4) eudicots arose during the last 30 million years, with the earliest before 22 Ma in Chenopodiaceae and Aizoaceae, and the latest probably after 2 Ma in Flaveria. C(4) eudicots are thus not globally younger than C(4) monocots. All lineages of C(4) plants evolved in a similar low CO(2) atmosphere that predominated during the last 30 million years. Independent C(4) origins were probably driven by different combinations of specific factors, including local ecological characteristics such as habitat openness, aridity, and salinity, as well as the speciation and dispersal history of each clade. Neither the lower number of C(4) species nor the frequency of C(3)-C(4) intermediates in eudicots can be attributed to a more recent origin, but probably result from variation in diversification and evolutionary rates among the different groups that evolved the C(4) pathway.

Shared origins of a key enzyme during the evolution of C4 and CAM metabolism

Summary Using phylogenetics and transcriptomics, we show that independent origins of both CAM and C4 photosynthesis in Caryophyllales co-opted the same genes for PEPC through similar adaptive changes.

Genetic enablers underlying the clustered evolutionary origins of C4 photosynthesis in angiosperms

The evolutionary accessibility of novel adaptations varies among lineages, depending in part on the genetic elements present in each group. However, the factors determining the evolutionary potential of closely related genes remain largely unknown. In plants, CO2-concentrating mechanisms such as C4 and crassulacean acid metabolism (CAM) photosynthesis have evolved numerous times in distantly related groups of species, and constitute excellent systems to study constraints and enablers of evolution. It has been previously shown for multiple proteins that grasses preferentially co-opted the same gene lineage for C4 photosynthesis, when multiple copies were present. In this work, we use comparative transcriptomics to show that this bias also exists within Caryophyllales, a distantly related group with multiple C4 origins. However, the bias is not the same as in grasses and, when all angiosperms are considered jointly, the number of distinct gene lineages co-opted is not smaller than that expected by chance. These results show that most gene lineages present in the common ancestor of monocots and eudicots produced gene descendants that were recruited into C4 photosynthesis, but that C4-suitability changed during the diversification of angiosperms. When selective pressures drove C4 evolution, some copies were preferentially co-opted, probably because they already possessed C4-like expression patterns. However, the identity of these C4-suitable genes varies among clades of angiosperms, and C4 phenotypes in distant angiosperm groups thus represent genuinely independent realizations, based on different genetic precursors.

A phylogenetic analysis of the genus Paspalum (Poaceae) based on cpDNA and morphology

With about 350 species, Paspalum is one of the richest genera within the Poaceae. Its species inhabit ecologically diverse areas along the Americas and they are largely responsible for the biodiversity of grassland ecosystems in South America. Despite its size and relevance, no phylogeny of the genus as a whole is currently available and infrageneric relationships remain uncertain. Many Paspalum species consist of sexual-diploid and apomictic-polyploid cytotypes, and several have arisen through hybridization. In this paper we explore the phylogenetic structure of Paspalum using sequence data of four non-coding cpDNA fragments from a wide array of species which were combined with morphological data for a subset of diploid taxa. Our results confirmed the general monophyly of Paspalum if P. inaequivalve is excluded and the small genus Thrasyopsis is included. Only one of the four currently recognized subgenera was monophyletic but nested within the remainder of the genus. Some informal morphological groups were found to be polyphyletic. The placement of known allopolyploid groups is generally congruent with previously stated hypotheses although some species with shared genomic formulae formed paraphyletic arrangements. Other species formed a basal grade including mostly umbrophilous or hygrophilous species. It is hypothesized that the genus may have diversified as a consequence of the expansion of C4 grass-dominated grasslands in South America.

Isolation and characterization of novel microsatellite markers for Arctium minus (Compositae)

UNLABELLED PREMISE OF THE STUDY Microsatellite primers were developed for the invasive plant Arctium minus to investigate the effects of facultative self-pollination and the biannual habit on population genetic structure, as well as the colonization of the Americas by this Eurasian species. • METHODS AND RESULTS Sixteen di- and trinucleotide microsatellite loci were identified in six populations. The number of alleles per locus ranged from one to 10, observed heterozygosities ranged from 0.000 to 0.897, and the mean value of F(IS) was 0.316. • CONCLUSIONS These results indicate the utility of these loci in future studies of population genetics in A. minus.

Characterization of polymorphic microsatellite loci in Haageocereus (Trichocereeae, Cactaceae)

UNLABELLED PREMISE OF THE STUDY Microsatellites were isolated from two species of the genus Haageocereus (H. tenuis and H. pseudomelanostele) to be applied in studies of genetic diversity and population structure. • METHODS AND RESULTS Five loci were employed in a preliminary study of genetic diversity and population differentiation in two rare (H. tenuis and H. repens) and two widespread (H. acranthus and H. pseudomelanostele) species, yielding between one and 44 alleles per locus. All five loci were polymorphic, with overall levels of observed and expected heterozygosities ranging from 0.478 to 0.871 and from 0.564 to 0.956, respectively. Three additional loci were scored in H. pseudomelanostele. These eight plus the remaining 11 loci were amplified from putative parents of three hybrids involving Haageocereus and Espostoa. • CONCLUSIONS These markers will facilitate analysis of genetic diversity, hybridization, and population differentiation throughout Haageocereus and Espostoa.

Genetic Variability of an Unusual Apomictic Triploid Cactus—Haageocereus tenuis Ritter—from the Coast of Central Peru

Haageocereus tenuis is a prostrate cactus restricted to a small area of 2 km(2) near the city of Lima, Peru. The species is triploid and propagates mainly through stem fragmentation. In addition, propagation via agamospermy is documented and adventitious embryony is also inferred as a mechanism. Although seedling recruitment has not been observed in nature, we have shown that asexually produced seeds are viable. About 45 adult individuals, plus 9 individuals obtained from seeds, were sampled and 5 microsatellite markers were used to assess genetic variability. Microsatellite analysis confirms that individuals from the only existing population are genetically identical and that the population likely represents a single clone. The absence of mutations in any individual, even in highly variable microsatellite loci, may indicate that the species is also of recent origin. Other prostrate species of Haageocereus are suspected to be occasional apomicts. This phenomenon has significant implications for the evolutionary biology and ecology of Haageocereus and other clonal Cactaceae.

Revealing a Cryptic Fern Distribution Through DNA Sequencing: Pityrogramma trifoliata in the Western Andes of Peru

Abstract Fern identification usually requires the use of mature sporophytes, since attempts to identify juveniles using morphological traits often provides unsatisfactory results. Here we examined young sporophytes found among boulders in a river basin of a xeric valley in central Peru. Attempts to identify these sporophytes first pointed to four different genera, two in Pteridaceae (Anogramma and Pityrogramma), and the others in Aspleniaceae (Asplenium) and Cystopteridaceae (Cystopteris). Here, we resolved this puzzle combining morphology and sequences of DNA (rbcL and trnG-R) that point to Pityrogramma trifoliata of Pteridaceae.

Characterization of 16 Microsatellite Markers for the Oreinotinus Clade of Viburnum (Adoxaceae)

Premise of the study: Microsatellite loci were isolated from four species of Viburnum (Adoxaceae) to study population structure and assess species boundaries among morphologically similar South American Viburnum species of the Oreinotinus clade. Methods and Results: Using a microsatellite-enriched library and mining next-generation sequence data, 16 microsatellites were developed. Each locus was tested on two populations of V. triphyllum and one population of V. pichinchense. For nuclear loci, one to 13 alleles were recovered, expected heterozygosity ranged from 0 to 0.8975, Simpson diversity index ranged from 0.0167 to 1.000, and Shannon diversity index ranged from 0 to 2.3670 in a given population. For the mitochondrial locus, three to six alleles were recovered and unbiased haploid diversity values ranged from 0.756 to 0.853 in a given population. Conclusions: The 16 microsatellite loci developed for the Oreinotinus clade (Viburnum, Adoxaceae) will inform investigations of population structure and species boundaries within this group.