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 tha...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.展开更多
基金supported by the National Natural Science Foundation of China(Grant No.32070242)the National Key Research and Development Program of China(Grant No.2020YFA0907900)+7 种基金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)the Science,Technology and Innovation Commission of Shenzhen Municipality of China(ZDSYS 20200811142605017)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)programOak Ridge National Laboratory is managed by UT-Battelle,LLC,for the U.S.Department of Energy under Contract Number DE-AC05-00OR22725support from the Scientific Research Foundation of Fairy Lake Botanical Garden No.2020-04.
文摘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.