Shared Expression of Crassulacean Acid Metabolism (CAM) Genes Pre-dates the Origin of CAM in the Genus Yucca

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2019 Mar 15

PMID 30870557

Citations 20

Authors

Karolina Heyduk

Jeremy N Ray

Saaravanaraj Ayyampalayam

Nida Moledina

Anne Borland

Scott A Harding

Chung-Jui Tsai

Jim Leebens-Mack

Affiliations

Soon will be listed here.

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 h period from both well-watered and drought-stressed plants, and were clustered based on time-dependent expression patterns. Metabolomic data reveal differences in carbohydrate metabolism and antioxidant response between the CAM and C3 species, suggesting that 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 C3Yucca species suggests that ancestral expression patterns required for CAM may have pre-dated its origin in Yucca.

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References

Abraham P, Yin H, Borland A, Weighill D, Lim S, De Paoli H . Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nat Plants. 2016; 2:16178. DOI: 10.1038/nplants.2016.178. View

Koch K . CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996; 47:509-540. DOI: 10.1146/annurev.arplant.47.1.509. View

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

Conesa A, Nueda M, Ferrer A, Talon M . maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics. 2006; 22(9):1096-102. DOI: 10.1093/bioinformatics/btl056. View

Taybi T, Nimmo H, Borland A . Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic capacity and phenotypic plasticity in the expression of crassulacean acid metabolism. Plant Physiol. 2004; 135(1):587-98. PMC: 429420. DOI: 10.1104/pp.103.036962. View

Yin H, Guo H, Weston D, Borland A, Ranjan P, Abraham P . Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave. BMC Genomics. 2018; 19(1):588. PMC: 6090859. DOI: 10.1186/s12864-018-4964-7. View

Adams W, Osmond C . Internal CO(2) Supply during Photosynthesis of Sun and Shade Grown CAM Plants in Relation to Photoinhibition. Plant Physiol. 1988; 86(1):117-23. PMC: 1054439. DOI: 10.1104/pp.86.1.117. View

Li B, Dewey C . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323. PMC: 3163565. DOI: 10.1186/1471-2105-12-323. View

Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P . Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev. 2000; 14(16):2085-96. PMC: 316855. View

10.

Dodd A, Griffiths H, Taybi T, Cushman J, Borland A . Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta. 2003; 216(5):789-97. DOI: 10.1007/s00425-002-0930-2. View

11.

Schulze S, Mallmann J, Burscheidt J, Koczor M, Streubel M, Bauwe H . Evolution of C4 photosynthesis in the genus flaveria: establishment of a photorespiratory CO2 pump. Plant Cell. 2013; 25(7):2522-35. PMC: 3753380. DOI: 10.1105/tpc.113.114520. View

12.

Haas B, Papanicolaou A, Yassour M, Grabherr M, Blood P, Bowden J . De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013; 8(8):1494-512. PMC: 3875132. DOI: 10.1038/nprot.2013.084. View

13.

Zhang J, Liu J, Ming R . Genomic analyses of the CAM plant pineapple. J Exp Bot. 2014; 65(13):3395-404. DOI: 10.1093/jxb/eru101. View

14.

Chen L, Lin Q, Nose A . A comparative study on diurnal changes in metabolite levels in the leaves of three crassulacean acid metabolism (CAM) species, Ananas comosus, Kalanchoë daigremontiana and K. pinnata. J Exp Bot. 2002; 53(367):341-50. DOI: 10.1093/jexbot/53.367.341. View

15.

Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J . Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell. 2013; 25(2):694-714. PMC: 3608787. DOI: 10.1105/tpc.112.106989. View

16.

Dever L, Boxall S, Knerova J, Hartwell J . Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiol. 2014; 167(1):44-59. PMC: 4281012. DOI: 10.1104/pp.114.251827. View

17.

Brilhaus D, Brautigam A, Mettler-Altmann T, Winter K, Weber A . Reversible Burst of Transcriptional Changes during Induction of Crassulacean Acid Metabolism in Talinum triangulare. Plant Physiol. 2015; 170(1):102-22. PMC: 4704576. DOI: 10.1104/pp.15.01076. View

18.

Langmead B, Trapnell C, Pop M, Salzberg S . Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25. PMC: 2690996. DOI: 10.1186/gb-2009-10-3-r25. View

19.

Leon P, Sheen J . Sugar and hormone connections. Trends Plant Sci. 2003; 8(3):110-6. DOI: 10.1016/S1360-1385(03)00011-6. View

20.

Kind T, Wohlgemuth G, Lee D, Lu Y, Palazoglu M, Shahbaz S . FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem. 2009; 81(24):10038-48. PMC: 2805091. DOI: 10.1021/ac9019522. View