Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis

Li, Cheng; Huang, Wenjie; Han, Xiaoxu; Zhao, Guohua; Zhang, Wenyang; He, Weijun; Nie, Bao; Chen, Xufeng; Zhang, Taijie; Bai, Wenhui; Zhang, Xiaopeng; He, Jingjing; Zhao, Cheng; Fernie, Alisdair R.; Tschaplinski, Timothy J.; Yang, Xiaohan; Yan, Shijuan; Wang, Li

doi:10.1016/j.xplc.2023.100594

Title: Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis

Journal Article · Thu Mar 23 00:00:00 EDT 2023 · Plant Communications

DOI:https://doi.org/10.1016/j.xplc.2023.100594· OSTI ID:1993667

Li, Cheng ^[1]; Huang, Wenjie ^[2]; Han, Xiaoxu ^[1]; Zhao, Guohua ^[3]; Zhang, Wenyang ^[2]; He, Weijun ^[1]; Nie, Bao ^[1]; Chen, Xufeng ^[2]; Zhang, Taijie ^[4]; Bai, Wenhui ^[1]; Zhang, Xiaopeng ^[1]; He, Jingjing ^[1]; Zhao, Cheng ^[1]; Fernie, Alisdair R. ^[5];

^[6];

^[6]; Yan, Shijuan ^[2];

^[1]

Chinese Academy of Agricultural Sciences, Shenzhen (China)
Guangdong Academy of Agricultural Sciences (China)
Chinese Academy of Science, Shenzhen (China)
Guangdong Provincial Key Laboratory of High Technology for Plant Protection (China)
Max Planck Institute of Molecular Plant Physiology (Germany)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Crassulacean acid metabolism (CAM) has high water-use efficiency (WUE) and is widely recognized to have evolved from C₃ photosynthesis. Different plant lineages have convergently evolved CAM, but the molecular mechanism that underlies C₃-to-CAM evolution remains to be clarified. Platycerium bifurcatum (elkhorn fern) provides an opportunity to study the molecular changes underlying the transition from C₃ to CAM photosynthesis because both modes of photosynthesis occur in this species, with sporotrophophyll leaves (SLs) and cover leaves (CLs) performing C₃ and weak CAM photosynthesis, respectively. Here, we report that the physiological and biochemical attributes of CAM in weak CAM-performing CLs differed from those in strong CAM species. We investigated the diel dynamics of the metabolome, proteome, and transcriptome in these dimorphic leaves within the same genetic background and under identical environmental conditions. We found that multi-omic diel dynamics in P. bifurcatum exhibit both tissue and diel effects. Our analysis revealed temporal rewiring of biochemistry relevant to the energy-producing pathway (TCA cycle), CAM pathway, and stomatal movement in CLs compared with SLs. We also confirmed that PHOSPHOENOLPYRUVATE CARBOXYLASE KINASE (PPCK) exhibits convergence in gene expression among highly divergent CAM lineages. Gene regulatory network analysis identified candidate transcription factors regulating the CAM pathway and stomatal movement. Taken together, our results provide new insights into weak CAM photosynthesis and new avenues for CAM bioengineering.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Natural Science Foundation of China (NSFC); National Key Research and Development Program of China; Shenzhen Science and Technology Program

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1993667

Journal Information:: Plant Communications, Vol. 4, Issue 5; ISSN 2590-3462

Publisher:: Cell PressCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Platycerium bifurcatum
crassulacean acid metabolism
multi-omics
transcription factor
PPCK
convergent evolution

Title: Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis

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