Altered Gene Regulatory Networks are Associated with the Transition from C₃ to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

Abstract

Crassulacean acid metabolism (CAM) photosynthesis is a modification of the core C3 photosynthetic pathway that improves the ability of plants to assimilate carbon in water-limited environments. CAM plants fix CO2 mostly at night, when transpiration rates are low. All of the CAM pathway genes exist in ancestral C3 species, but the timing and magnitude of expression are greatly altered between C3 and CAM species. Understanding these regulatory changes is key to elucidating the mechanism by which CAM evolved from C3. Here we use two closely related species in the Orchidaceae, Erycina pusilla (CAM) and Erycina crista-galli (C3), to conduct comparative transcriptomic analyses across multiple time points. Clustering of genes with expression variation across the diel cycle revealed some canonical CAM pathway genes similarly expressed in both species, regardless of photosynthetic pathway. However, gene network construction indicated that 149 gene families had significant differences in network connectivity and were further explored for these functional enrichments. Genes involved in light sensing and ABA signaling were some of the most differently connected genes between the C3 and CAM Erycina species, in agreement with the contrasting diel patterns of stomatal conductance in C3 and CAM plants. Our results suggest changes to transcriptional cascades are important for the transition from C3 to CAM photosynthesis in Erycina.

Kalanchoë PPC1 Is Essential for Crassulacean Acid Metabolism and the Regulation of Core Circadian Clock and Guard Cell Signaling Genes

“…The GCs of CAM leaves and stems are thought to respond directly to the internal supply of CO 2 . This theory has recently led several groups to use whole leaf RNA-seq datasets to investigate alterations, relative to C 3 leaves, in the temporal phasing of known GC regulatory genes and membrane transporters (Abraham et al, 2016;Wai and VanBuren, 2018;Yin et al, 2018;Heyduk et al, 2019;Moseley et al, 2019). However, these studies did not use intact GCs.…”

Undervalued potential of crassulacean acid metabolism for current and future agricultural production

“…The relatively recent publication of CAM genomes (Ming et al , 2015) and CAM physiological models (e.g. Owen and Griffiths, 2013) is providing a platform to direct engineering towards optimization of current CAM crops through identification and selection of genes controlling traits of interest (Heyduk et al , 2018; Lim et al , 2019).…”

“…Tsai et al (2017) highlight the progress in orchid genomics research, with interesting developments that include transcriptome data investigating pod development in the prized vanilla orchid, Vanilla planifolia (Rao et al , 2014), and whole genome sequencing for the moth orchid Phalaenopsis equestris (Cai et al , 2015; Albert and Carretero-Paulet, 2015). Heyduk et al (2018) used comparative transcriptomics to determine gene expression difference between CAM and C 3 species of orchids in the Erycina genus that are closely related.…”

“…Cascading transcriptional changes are further described as fundamental for the expression of CAM in Erycina spp. (Heyduk et al , 2018). Experimental approaches are now required to investigate the effects of the C 3 -to-CAM transition and to determine the potential for accelerating crop improvement.…”

Evolution of Crassulacean Acid Metabolism (CAM) as an escape from ecological niche conservatism in MalagasyBulbophyllum(Orchidaceae)

“…CC-BY 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made The copyright holder for this preprint this version posted January 9, 2021. ; https://doi.org/10.1101/2021.01.09.426039 doi: bioRxiv preprint Heyduk et al 2019). CAM occurs in many succulent species of warm, semi-arid regions (e.g.…”