Phylogenomics in Cactaceae: A case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan and Sonoran deserts

Abstract

Premise Although numerous phylogenetic studies have been conducted in Cactaceae, whole‐plastome datasets have not been employed. We used the chollas to develop a plastome dataset for phylogeny reconstruction to test species relationships, biogeography, clade age, and morphological evolution. Methods We developed a plastome dataset for most known diploid members of the chollas (42 taxa) as well as for other members of Cylindropuntieae. Paired‐end, raw reads from genome skimming were reference‐mapped onto a de novo plastome assembly of one species of cholla, Cylindropuntia bigelovii, and were used to build our plastome dataset, which was analyzed using various methods. Results Our plastome dataset resolved the phylogeny of the chollas, including most interspecific and intraspecific relationships. Tribe Cylindropuntieae arose ~18 mya, during the early Miocene in southern South America, and is supported as sister to the South American clade Tephrocacteae. The (Micropuntia (Cylindropuntia + Grusonia)) clade most likely originated in the Chihuahuan Desert region around 16 mya and then migrated into other North American desert regions. Key morphological characters for recognizing traditional taxonomic series in Cylindropuntia (e.g., spiny fruit) are mostly homoplasious. Conclusions This study provides the first comprehensive plastome phylogeny for any clade within Cactaceae. Although the chollas s.l. are widespread throughout western North American deserts, their most recent common ancestor likely arose in the Chihuahuan Desert region during the mid‐Miocene, with much of their species diversity arising in the early to mid‐Pliocene, a pattern strikingly similar to those found in other western North American desert groups.

Insights Into Chloroplast Genome Evolution Across Opuntioideae (Cactaceae) Reveals Robust Yet Sometimes Conflicting Phylogenetic Topologies

“…Members of Cactaceae also have experienced different alterations in their chloroplast genome. A conserved inversion of ∼6 kb on the large single copy unit comprising the trnM-rbcL genes have long been suggested (Wallace, 1995) and more recently confirmed (Sanderson et al, 2015;Majure et al, 2019;Solórzano et al, 2019). Besides that, the first cactus plastome assembled from the saguaro cactus [Carnegiea gigantea (Engelm.)…”

“…Opuntioideae (∼350 spp.) is the most widespread subfamily with members occurring from southern South America (Argentina) to northern North America (Canada) (Britton and Rose, 1919;Anderson, 2001;Hunt et al, 2006;Ritz et al, 2012;Majure and Puente, 2014;Majure et al, 2019). The group shows interesting morphological synapomorphies, such as the small brushlike, barbed spines (i.e., glochids) and a bony aril surrounding a campylotropous ovule (Stuppy, 2002;Taylor et al, 2002).…”

“…While Doweld (1999) and Wallace and Dickie (2002) proposed five tribes, with different circumscriptions from each otherfour were recognized as monophyletic in the last comprehensive molecular study of Opuntioideae (Griffith and Porter, 2009). Despite great improvement in our phylogenetic understanding in Opuntioideae (Griffith and Porter, 2009;Ritz et al, 2012;Majure et al, 2019), support for the relationships among those clades, as well as a better taxon sampling with more molecular markers, still needs to be strengthened.…”

“…NGS data are also showing to be extremely useful for discovering informative regions across genomes, for marker development (Wu et al, 2010;Dong et al, 2012;Ripma et al, 2014;Reginato et al, 2016;Abdullah et al, 2019), as well as to investigate chloroplast genome evolution (Dong et al, 2013;Mower and Vickrey, 2018;Yao et al, 2019). Nevertheless, this approach is still in its infancy across Cactaceae (Majure et al, 2019) and remains a path to be explored.…”

Diverse genomoviruses representing twenty-nine species identified associated with plants

“…Cacti have undergone adaptive radiations across a wide variety of edaphically dry environments [1,2], which, together with high degrees of phenotypic diversification within the family, have yielded a broad range of morphological forms [3,4]. Phylogenetic relationships in the family are relatively well-known, and four principle clades have been recovered in analyses (Leuenbergeria, Pereskia, Cactoideae + Maihuenia, and Opuntioideae) [2,5,6]. Cacti are culturally, economically and ecologically important [7].…”