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Clusia genomes shed light on the evolution and diversity of CAM physiotypes

ABSTRACT:

225 years ago, Alexander von Humboldt observed the first crassulacean acid metabolism (CAM) tree, Clusia rosea (Clusiaceae). Since then, the photosynthetic and ecophysiological plasticity of Clusia

species have captivated the minds of plant scientists worldwide. CAM is a physiological adaptation to low water availability. While stomata are closed during the day, RuBisCO is supplied with CO2 via

decarboxylation of organic acids that have been stored and synthesized during the night by phosphoenolpyruvate carboxylases (PEPC). How the physiological reprogramming necessary for CAM

evolved remains enigmatic. Photosynthetic physiotypes of CAM, including weak CAM, inducible CAM, and CAM-cycling have additionally fueled a debate on the evolutionary constraints of CAM and the prospects of engineering CAM into C3 crops. Here, we de novo sequenced the genomes of three Clusia species to capture genetic snapshots along an evo-ecophysiological continuum from weak over inducible to strong CAM. Through a combination of phased chromosome level assembly and annotation, comparative multiomics, and physiological experiments, we demonstrate that diploidization of polyploids explains the physiotype diversity of CAM. We illustrate that Clusia major, a plant that exhibits a C3-type mode of photosynthesis, retained almost all hallmarks of CAM. Transposon-mediated genic diploidization, however, acted upon homoeologs in CAM-related gene families, preferentially those involved in phosphoenolpyruvate (PEP) recycling via phosphorolytic leaf starch metabolization. In effect this rendered a plant capable of constitutive C3+CAM with open stomata during the day by shifting carbohydrate supply (PEP) to viable soluble sugars. Our findings indicate that polyploidization during genus evolution and subsequent diploidization shaped the emergence of extant C3+CAM physiotypes in Clusia. This study of evolutionary intermediates provides crucial insights into the convergent evolution of physiotype diversity and plasticity of CAM.

INSTRUMENT(S): Gas Chromatography MS - positive

PROVIDER: MTBLS14075 | MetaboLights | 2026-03-23

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS14075_GC-MS_positive__metabolite_profiling.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS14075_GC-MS_positive__metabolite_profiling_v2_maf.tsv	Tabular
	s_MTBLS14075.txt	Txt

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Project description:225 years ago, Alexander von Humboldt documented his first observations of a peculiar phenomenon in Clusia rosea (Clusiaceae), the first tree known to perform crassulacean acid metabolism (CAM). Since then, the photosynthetic and ecophysiological plasticity of Clusia species have captivated the minds of plant scientists worldwide. CAM is a physiological adaptation to low water availability. While stomata are closed during the day, RuBisCO is supplied with CO2 via decarboxylation of organic acids that have been stored and synthesized during the night by phosphoenolpyruvate carboxylases (PEPC). How the physiological reprogramming necessary for CAM evolved remains enigmatic. Photosynthetic physiotypes of CAM, including weak CAM, inducible CAM, and CAM-cycling have additionally fueled a debate on the evolutionary constraints of CAM and the prospects of engineering CAM into C3 crops. Here, we de novo sequenced the genomes of three Clusia species to capture genetic snapshots along an evo-ecophysiological continuum from weak over inducible to strong CAM. Through a combination of phased chromosome level assembly and annotation, comparative multiomics, and physiological experiments, we demonstrate that diploidization of polyploids explains the physiotype diversity of CAM. We illustrate that Clusia major, a plant that exhibits a C3-type mode of photosynthesis, retained almost all hallmarks of CAM. Transposon-mediated genic diploidization, however, acted upon homoeologs in CAM-related gene families, preferentially those involved in phosphoenolpyruvate (PEP) recycling via phosphorolytic leaf starch metabolization. In effect this rendered a plant capable of constitutive C3+CAM with open stomata during the day by shifting carbohydrate supply (PEP) to viable soluble sugars. Our findings indicate that polyploidization during genus evolution and subsequent diploidization shaped the emergence of extant C3+CAM physiotypes in Clusia. This study of evolutionary intermediates provides crucial insights into the convergent evolution of physiotype diversity and plasticity of CAM.

Project description:The resurrection plant Craterostigma plantagineum possesses an extraordinary capacity to survive long-term desiccation. To enhance our understanding of this phenomenon, complementary transcriptome, soluble proteome and primary metabolome analyses were carried out on plant leaves collected from different physiological stages during a dehydration and rehydration cycle. A total of 7348 contigs, 611 proteins and 46 metabolites were differentially regulated across stages. Dynamic changes in transcript, protein and metabolite levels revealed a unique signature characterizing each stage. An overall low correlation between transcript and protein abundance suggests a prominent role for post-transcriptional modification in metabolic reprogramming to prepare plants to desiccation and recovery upon rehydration. The integrative analysis of three -omics datasets was performed with an emphasis on photosynthesis, photorespiration, energy metabolism and amino acid metabolism. The results revealed a set of fine regulations/changes that modulate primary metabolism to confer plasticity to metabolic pathways, thus optimizing plant performance under stress. For example, maintenance of cyclic electron flow and photorespiration and switch from C3 to Crassulacean acid metabolism (CAM) photosynthesis may contribute to partially sustain photosynthesis and minimize oxidative damage during dehydration. transcripts with a delayed translation, ATP-independent bypasses, alternative respiratory pathway and 4-aminobutyric acid (GABA) shunt may play a role in energy management, altogether conferring bioenergetic advantages to meet energy demands for survival during desiccation. This knowledge provides a high-resolution map of the changes occurring in the primary metabolism during dehydration and rehydration and enriches the current understanding of the molecular mechanisms underpinning plant desiccation tolerance. The datasets here provided will ultimately inspire biotechnological strategies for drought tolerance improvement in crops.

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Clusia genomes shed light on the evolution and diversity of CAM physiotypes

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