Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation

Abstract

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or "key innovations" including the transition from C 3 to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C 3 /CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C 3 /CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar-and light-dependent regulation of growth and development. Our analyses also support the reprogramming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.

Genome Skimming Reveals Widespread Hybridization in a Neotropical Flowering Plant Radiation

“…Bias toward reference allele due to alignment also can have an effect on SNP calling, even if it was shown to be negligible with genome skimming on pigs (Ros-Freixedes et al, 2018). To limit this bias, we used the Tillandsia adpressiflora pseudo-reference genome constructed in de la Harpe et al (2020) for mapping our samples. The method consisted in incorporating specific variation of a T. adpressiflora individual sequenced at high coverage into the high quality Ananas comosus genome (Ming et al, 2015).…”

Taxon-specific or universal? Using target capture to study the evolutionary history of rapid radiations

“…The bait subset of genes associated with key innovative traits in Bromeliaceae (subset ii above) included (1) genes putatively under positive selection along branches relevant to C3/CAM shifts (de La Harpe et al, 2020), (2) genes that exhibit differential gene expression between CAM and C3 Tillandsia species (de La Harpe et al, 2020) and (3) genes putatively associated with photosynthetic and developmental functions, or with flavonoid and antho-cyanin biosynthesis, according to the literature (e.g. Ming et al, 2015; Palma-Silva, Ferro, Bacci, & Turchetto-Zolet, 2016; Wai et al, 2017; Goolsby, Moore, Hancock, Vos, & Edwards, 2018).…”

“…Finally, we used a draft genome of T. fasciculata (Jaqueline Hess, personal communication) to exclude from all candidates genes that exhibited multiple BLASTN hits, if they have not been previously described as duplicated within the genus (de La Harpe et al, 2020). Specifically, we excluded genes that matched another genomic sequence of at least 100bp with high similarity score (> 80%) and low E-value (< 10 −5 ).…”

“…Finally, we used a draft genome of T. fasciculata (Jaqueline Hess, personal communication) to exclude from all candidates genes that exhibited multiple BLASTN hits, if they have not been previously described as duplicated within the genus (de La Harpe et al, 2020).…”

“…CAM phenotypes are considered key adaptations in Bromeliaceae, associated with expansion into novel ecological niches. In Tillandsia, C3/CAM shifts were found to be particularly associated with increased rates of diversification (Crayn et al, 2004;de La Harpe et al, 2020;Givnish et al, 2014). The Bromeliad1776 bait set offers opportunities to address specific questions on the relationship between rapid diversification and photosynthetic syndromes in this clade, including testing for gene sequence evolution.…”