Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism

Heyduk, Karolina; Ray, Jeremy N.; Ayyampalayam, Saravanaraj; Leebens‐Mack, James H.

doi:10.1002/ajb2.1017

Cited by 38 publications

(56 citation statements)

References 80 publications

(93 reference statements)

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“…Secondly, CAM has evolved many times independently and it is believed to be present in well over 5% of vascular plant species 42,43 . These observations can be attributed to the fact that CAM most likely evolved on a ‘biochemistry first, anatomy second’ trajectory 44 in which ‘C 3 +CAM’ is an evolutionarily accessible phenotype on the trajectory to strong CAM 45,46 . Our model demonstrates the water-saving potential of a partial CAM or CAM-like mode for plants grown in temperate climates, while maintaining a high net metabolic output.…”

Section: Discussionmentioning

confidence: 99%

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

Toepfer

Braam

Shameer

et al. 2020

Preprint

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11Crassulacean Acid Metabolism (CAM) evolved in arid environments as a water-saving 12 alternative to C3 photosynthesis. There is great interest in engineering more drought-resistant 13 crop species by introducing CAM into C3 plants. However, one of the open questions is 14 whether full CAM or alternative water-saving flux modes would be more productive in the 15 environments typically experienced by C3 crops. To study the effect of temperature and 16relative humidity on plant metabolism we coupled a time-resolved diel model of leaf 17 metabolism to an environment-dependent gas-exchange model. This model allowed us to 18 study the emergence of CAM or CAM-like behaviour as a result of a trade-off between leaf 19 productivity and water-saving. We show that vacuolar storage capacity in the leaf is a major 20 determinant of the extent of CAM and shapes the occurrence of phase II and IV of the CAM 21 cycle. Moreover, the model allows us to study alternative flux routes and we identify 22 mitochondrial isocitrate dehydrogenase (ICDH) and an isocitrate-citrate-proline-2OG cycle as 23 a potential contributor to initial carbon fixation at night. Simulations across a wide range of 24 environmental parameters show that the water-saving potential of CAM strongly depends on 25 the environment and that the additional water-saving effect of carbon fixation by ICDH can 26 reach up to 4% for the conditions tested. 27 28 An optimality study reveals trade-offs between productivity and WUE 131Computationally, the question of how a system's behaviour changes when operating between 132 competing objectives can be tackled by performing a Pareto analysis [16][17][18][19] . In our case phloem 133 output and water-saving represented two competing driving forces. We started the Pareto 134 analysis from the above described scenario of a mature leaf optimized for maximum phloem 135 output (i.e. 100% phloem output, here termed Pareto step 1). We then subsequently reduced 136 the required phloem output in 10%-steps and used minimization of water loss as the primary 137 optimization objective. Given this setup, we saw an almost linear decrease in water loss with 138 decreasing phloem output, hence we did not observe any significant water-saving mechanism 139

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Section: Discussionmentioning

confidence: 99%

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

Toepfer

Braam

Shameer

et al. 2020

Preprint

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“…Our understanding of the genetics and genome structure of CAM has come predominantly from studies that involve comparisons between C 3 and CAM tissues sampled from evolutionarily distant species, or from samples taken from one species under different age or environmental conditions (Taybi et al , 2004; Cushman et al , 2008 b ; Gross et al , 2013; Brilhaus et al , 2016) (but see (Heyduk et al , 2017)). Recent studies have profiled gene expression before and after CAM induction in Mesembryanthemum crystallinum (Cushman et al , 2008 b ) and in Talinum (Brilhaus et al , 2016).…”

Section: Introductionmentioning

confidence: 99%

Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genusYucca

Heyduk¹,

Ray²,

Ayyampalayam³

et al. 2018

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Title: Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genus Yucca. Running title: Shared gene expression in C3 and CAM Yucca speciesHighlight: Although large differences in metabolism exist between C3 and CAM species, we find that many CAM genes have shared expression patterns regardless of photosynthetic pathway, suggesting ancestral propensity for CAM.Abstract: Crassulacean acid metabolism (CAM) is a carbon-concentrating mechanism that has evolved numerous times across flowering plants and is thought to be an adaptation to water limited environments. CAM has been investigated from physiological and biochemical perspectives, but little is known about how plants evolve from C3 to CAM at the genetic or metabolic level. Here we take a comparative approach in analyzing time-course data of C3, CAM, and C3+CAM intermediate Yucca (Asparagaceae) species. RNA samples were collected over a 24-hour period from both well-watered and drought-stressed plants and were clustered based on time-dependent expression patterns. Metabolomic data reveals differences in carbohydrate metabolism and antioxidant response between the CAM and C3 species, suggesting changes to metabolic pathways are important for CAM evolution and function. However, all three species share expression profiles of canonical CAM pathway genes, regardless of photosynthetic pathway. Despite differences in transcript and metabolite profiles between the C3 and CAM species, shared time-structured expression of CAM genes in both CAM and C3 Yucca species suggests ancestral expression patterns required for CAM may have predated its origin in Yucca.Introduction 1 Crassulacean acid metabolism (CAM) is a carbon concentrating mechanism that can 2 reduce photorespiration and enhance water use efficiency relative to plants that rely solely on the 3 C3 photosynthetic pathway. In CAM plants, stomata are open for gas exchange at night, when 4 transpiration rates are lower, and incoming CO2 is initially fixed by phosphoenolpyruvate 5 carboxylase (PEPC) rather than RuBisCO. Carbon is temporarily stored as malic acid within the 6 vacuole, and during the day stomata close and the malic acid is decarboxylated in the cytosol, 7 ultimately resulting in high concentrations of CO2 around RuBisCO. The extra steps of CAM -8 carboxylation of PEP, decarboxylation of malic acid, transport into and out of the vacuole -9come with extra energetic costs relative to C3 photosynthesis, but CAM plants have the 10 advantage of acquiring carbon with increased water use efficiency (WUE). In addition, RuBisCO 11 is able to act more efficiently with a high concentration of CO2 and the risk of photorespiration is 12 thought to be significantly minimized (Cushman and Bohnert, 1997; Schulze et al., 2013). CAM 13 plants are therefore adapted to habitats where water stress is unavoidable and where the energetic 14 cost of CAM is offset by reduced photorespiration under water limited conditions. CAM has 15 evolved at least 35 independent times in flowering plan...

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“…Recently, genome, transcriptome, proteome, and metabolome datasets for a phylogenetically diverse range of independent CAM origins have started to open up a large catalogue of putative CAM genes. CAM species represented by published 'omics datasets span orchids (Phalaenopsis equestris and Erycina pusilla, Orchidaceae, monocots), pineapple (Ananas comosus, Bromeliaceae, monocots), Agave (A. americana, A. deserti, A. tequilana, Agavaceae, monocots), Yucca (Y. aloifolia, Asparagaceae, monocots), Kalanchoë (K. fedtschenkoi and K. laxiflora, Crassulaceae, dicots), Mesembryanthemum (M. crystallinum, Aizoaceae, dicots), and Talinum (T. triangulare, Portulacaceae, dicots) (Cushman et al, 2008;Gross et al, 2013;Cai et al, 2015;Ming et al, 2015;Abraham et al, 2016;Brilhaus et al, 2016;Hartwell et al, 2016;Yang et al, 2017;Heyduk et al, 2018;Heyduk et al, 2019). The optimal exploitation of CAM will be facilitated through decoding the molecular-genetic blueprint for CAM from these genomes and transcriptomes.…”

Section: Introductionmentioning

confidence: 99%

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

Boxall

Kadu

Dever

et al. 2019

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Short Title: Silencing PPC1 in an obligate CAM plant One Sentence Summary: Silencing phosphoenolpyruvate carboxylase in an obligate CAM species prevented dark period CO2 fixation and malate accumulation, caused arrhythmia of some components within the central circadian clock and enhanced rhythms of others, and adjusted the temporal regulation and relative abundance of guard cell signalling genes. ABSTRACT Unlike C3 plants, Crassulacean acid metabolism (CAM) plants fix CO2 in the dark using phosphoenolpyruvate carboxylase (PPC; EC 4.1.1.31). PPC combines PEP with CO2(as HCO3 -), forming oxaloacetate that is rapidly converted to malate, leading to vacuolar malic acid accumulation that peaks phased to dawn. In the light period, malate decarboxylation concentrates CO2 around RuBisCO for secondary fixation.CAM mutants lacking PPC have not been described. Here, RNAi was employed totranscripts, PPC activity, dark period CO2 fixation, and nocturnal malate accumulation.Light period stomatal closure was also perturbed, and the plants displayed reduced but detectable dark period stomatal conductance, and arrhythmia of the CAM CO2 fixation circadian rhythm under constant light and temperature (LL) free-running conditions. By contrast, the rhythm of delayed fluorescence was enhanced in plants lacking PPC1. Furthermore, a subset of gene transcripts within the central circadian oscillator were up-regulated and oscillated robustly. The regulation guard cell genes involved controlling stomatal movements was also altered in rPPC1-B. This provided direct evidence that altered regulatory patterns of key guard cell signaling genes are linked with the characteristic inverse pattern of stomatal opening and closing during CAM. RESULTS Initial Screening and Characterisation of PPC1 RNAi Lines of K. laxifloraAs K. laxiflora is relatively slow to grow, flower and set seed, taking around 9-months seed-to-seed (Hartwell et al., 2016), data are presented for independent primary transformants that were propagated clonally via leaf margin plantlets and/ or stem cuttings. Primary transformants were screened initially using high-throughput leaf disc tests for starch and acidity at dawn and dusk (Cushman et al., 2008; Dever et al., 2015). Independent transgenic lines that acidified less during the dark period were screened for the steady-state abundance of PPC1 transcripts using RT-qPCR. Line rPPC1-B displayed a complete loss of PPC1 transcripts, whereas rPPC1-A had an intermediate level of PPC1 transcripts ( Figure 1A). The other plant-type PPC genes (PPC2, PPC3 and PPC4) were up-regulated relative to the wild type, with their peak

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Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism

Cited by 38 publications

References 80 publications

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genusYucca

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

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Shifts in gene expression profiles are associated with weak and strong Crassulacean acid metabolism

Cited by 38 publications

References 80 publications

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genusYucca

SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C3-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes

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SilencingPHOSPHOENOLPYRUVATE CARBOXYLASE1in the Obligate Crassulacean Acid Metabolism SpeciesKalanchoë laxifloracauses Reversion to C₃-like Metabolism and Amplifies Rhythmicity in a Subset of Core Circadian Clock Genes