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

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

doi:10.1016/j.xplc.2023.100594

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

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

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

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.

Original language	English
Article number	100594
Journal	Plant Communications
Volume	4
Issue number	5
DOIs	https://doi.org/10.1016/j.xplc.2023.100594
State	Published - Sep 11 2023

Funding

This study was supported by the National Natural Science Foundation of China (Grant No. 32070242 ), the National Key Research and Development Program of China (Grant No. 2020YFA0907900 ), the Shenzhen Science and Technology Program (Grant No. KQTD2016113010482651 ), special funds for science technology innovation and industrial development of Shenzhen Dapeng New District (Grant No. RC201901-05 and Grant No. PT201901-19 ), the Postdoctoral Research Foundation of China (Grant No. 2020M672904 ), the Basic and Applied Basic Research Fund of Guangdong (Grant No. 2020A1515110912 ), and the Science, Technology and Innovation Commission of Shenzhen Municipality of China (ZDSYS 20200811142605017 ). X.Y. acknowledges support from the Center for Bioenergy Innovation , a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under Contract Number DE-AC05-00OR22725 . G.Z. acknowledges support from the Scientific Research Foundation of Fairy Lake Botanical Garden No. 2020-04 .

Funders	Funder number
Scientific Research Foundation of Fairy Lake Botanical Garden	2020-04
U.S. Department of Energy
Biological and Environmental Research
Oak Ridge National Laboratory	DE-AC05-00OR22725
Center for Bioenergy Innovation
National Natural Science Foundation of China	32070242
Postdoctoral Research Foundation of China	2020M672904
Science, Technology and Innovation Commission of Shenzhen Municipality	KQTD2016113010482651, ZDSYS 20200811142605017
National Key Research and Development Program of China	2020YFA0907900
Basic and Applied Basic Research Foundation of Guangdong Province	2020A1515110912
special funds for science technology innovation and industrial development of Shenzhen Dapeng New District	PT201901-19, RC201901-05

Keywords

PPCK
Platycerium bifurcatum
convergent evolution
crassulacean acid metabolism
multi-omics
transcription factor

Access to Document

10.1016/j.xplc.2023.100594

Cite this

Li, C., Huang, W., Han, X., Zhao, G., Zhang, W., He, W., Nie, B., Chen, X., Zhang, T., Bai, W., Zhang, X., He, J., Zhao, C., Fernie, A. R., Tschaplinski, T. J., Yang, X., Yan, S., & Wang, L. (2023). Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis. Plant Communications, 4(5), Article 100594. https://doi.org/10.1016/j.xplc.2023.100594

@article{aba193b0ad6049cf84c09ee88ca92b2f,

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

abstract = "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.",

keywords = "PPCK, Platycerium bifurcatum, convergent evolution, crassulacean acid metabolism, multi-omics, transcription factor",

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

note = "Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = sep,

day = "11",

doi = "10.1016/j.xplc.2023.100594",

language = "English",

volume = "4",

journal = "Plant Communications",

issn = "2590-3462",

number = "5",

}

TY - JOUR

T1 - Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis

AU - Li, Cheng

AU - Huang, Wenjie

AU - Han, Xiaoxu

AU - Zhao, Guohua

AU - Zhang, Wenyang

AU - He, Weijun

AU - Nie, Bao

AU - Chen, Xufeng

AU - Zhang, Taijie

AU - Bai, Wenhui

AU - Zhang, Xiaopeng

AU - He, Jingjing

AU - Zhao, Cheng

AU - Fernie, Alisdair R.

AU - Tschaplinski, Timothy J.

AU - Yang, Xiaohan

AU - Yan, Shijuan

AU - Wang, Li

PY - 2023/9/11

Y1 - 2023/9/11

N2 - 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.

AB - 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.

KW - PPCK

KW - Platycerium bifurcatum

KW - convergent evolution

KW - crassulacean acid metabolism

KW - multi-omics

KW - transcription factor

UR - http://www.scopus.com/inward/record.url?scp=85160294049&partnerID=8YFLogxK

U2 - 10.1016/j.xplc.2023.100594

DO - 10.1016/j.xplc.2023.100594

M3 - Article

C2 - 36960529

AN - SCOPUS:85160294049

SN - 2590-3462

VL - 4

JO - Plant Communications

JF - Plant Communications

IS - 5

M1 - 100594

ER -

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

Abstract

Funding

Keywords

Access to Document

Other files and links

Fingerprint

Cite this