The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Yang, Xiaohan ^a,b   Hu, Rongbin ^a   Yin, Hengfu ^a   Jenkins, Jerry ^c   Shu, Shengqiang ^d   Tang, Haibao ^e   Liu, Degao ^a   Weighill, Deborah A ^a,b   Cheol Yim, Won ^f   Ha, Jungmin ^f   Heyduk, Karolina ^g   Goodstein, David M ^d   Guo, Hao Bo ^b   Moseley, Robert C ^a,b   Fitzek, Elisabeth ^h   Jawdy, Sara ^a   Zhang, Zhihao ^a   Xie, Meng ^a   Hartwell, James ⁱ   Grimwood, Jane ^c   Abraham, Paul E ^a   Mewalal, Ritesh ^a   Beltrán, Juan D ^j   Boxall, Susanna F ⁱ   Dever, Louisa V ⁱ   Palla, Kaitlin J ^a,b   Albion, Rebecca ^f   Garcia, Travis ^f   Mayer, Jesse A ^f   Don Lim, Sung ^f   Man Wai, Ching ^k   Peluso, Paul ^l   Van Buren, Robert ^m   De Paoli, Henrique Cestari ^a,b   Borland, Anne M ^a,n   Guo, Hong ^b   Chen, Jin Gui ^a   Muchero, Wellington ^a   Yin, Yanbin ^h   Jacobson, Daniel A ^a,b   Tschaplinski, Timothy J ^a   Hettich, Robert L ^a   Ming, Ray ^e,k   Winter, Klaus ^o   Leebens Mack, James H ^g   Smith, J Andrew C ^j   Cushman, John C ^f   Schmutz, Jeremy ^c,d   Tuskan, Gerald A ^a   more..

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^f UNIVERSITY OF NEVADA   (United States)

^g UNIVERSITY OF GEORGIA   (United States)

^h NORTHERN ILLINOIS UNIVERSITY   (United States)

ⁱ UNIVERSITY OF LIVERPOOL   (United Kingdom)

^j UNIVERSITY OF OXFORD   (United Kingdom)

^k UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^l PACIFIC BIOSCIENCES   (United States)

^m MICHIGAN STATE UNIVERSITY   (United States)

ⁿ NEWCASTLE UNIVERSITY   (United Kingdom)

^o SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ACID; CARBON DIOXIDE; WATER;

C3 PLANT; CIRCADIAN RHYTHM; CRASSULACEAN ACID METABOLISM; GENE EXPRESSION; GENOME; HYPOTHESIS TESTING; PHOTOSYNTHESIS; PROTEIN; WATER USE EFFICIENCY;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CARBOHYDRATE METABOLISM; CIRCADIAN RHYTHM; COMPARATIVE STUDY; CONVERGENT EVOLUTION; CRASSULACEAN ACID METABOLISM PLANT; DECARBOXYLATION; DNA SEQUENCE; DUPLICATE GENE; GENE DUPLICATION; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC CODE; GENETIC IDENTIFICATION; GENOME; GENOME SIZE; GENOME-WIDE ASSOCIATION STUDY; HEAT TOLERANCE; KALANCHOE; NONHUMAN; PHOTOSYNTHESIS; PHYLOGENETIC TREE; PLANT LEAF; PLANT WATER USE; PROTEIN PHOSPHORYLATION; CLASSIFICATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PLANT; PLANT GENOME;

CORE EUDICOTYLEDONS; CRASSULACEAE; MAGNOLIOPHYTA;

ACIDS; CARBON DIOXIDE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; KALANCHOE; PHOTOSYNTHESIS; PHYLOGENY; PLANTS; WATER;

EID: 85036668202     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-01491-7     Document Type: Article

References (79)

1. West-Eberhard, M., Smith, J. , Winter, K. Photosynthesis, reorganized. Science 332, 311-312 (2011).
2. Borland, A. M., Griffiths, H., Hartwell, J. , Smith, J. A. C. Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. J. Exp. Bot. 60, 2879-2896 (2009).
3. Cushman, J. C., Davis, S. C., Yang, X. , Borland, A. M. Development and use of bioenergy feedstocks for semi-arid and arid lands. J. Exp. Bot. 66, 4177-4193 (2015).
4. Yang, X., et al. A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytol. 207, 491-504 (2015).
5. Owen, N. A. , Griffiths, H. A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases. New Phytol. 200, 1116-1131 (2013).
6. Borland, A. M., et al. Engineering crassulacean acid metabolism to improve water-use efficiency. Trends Plant Sci. 19, 327-338 (2014).
7. Silvera, K., et al. Evolution along the crassulacan acid metabolism continuum. Funct. Plant Biol. 37, 995-1010 (2010).
8. Christopher, J. , Holtum, J. Patterns of carbohydrate partitioning in the leaves of crassulacean acid metabolism species during deacidification. Plant Physiol. 112, 393-399 (1996).
9. Holtum, J. A. M., Smith, J. A. C. , Neuhaus, H. E. Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Funct. Plant Biol. 32, 429-449 (2005).
10. Washburn, J. D., Bird, K. A., Conant, G. C., Pires, J. C. , Herendeen, P. S. Convergent evolution and the origin of complex phenotypes in the age of systems biology. Int. J. Plant Sci. 177, 305-318 (2016).
11. Morris S. C. Life's Solution: Inevitable Humans In A Lonely Universe. Cambridge University (2003).
12. Foote, A. D., et al. Convergent evolution of the genomes of marine mammals. Nat. Genet. 47, 272-275 (2015).
13. Hu, Y. B., et al. Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc. Natl Acad. Sci. USA 114, 1081-1086 (2017).
14. Natarajan, C., et al. Predictable convergence in hemoglobin function has unpredictable molecular underpinnings. Science 354, 336-339 (2016).
15. Gould S. J. Wonderful Life: The Burgess Shale And The Nature Of Life. Norton (1989).
16. Pfenning, A. R., et al. Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346, 1256846 (2014).
17. Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L. L. , Hernández-Hernández, T. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207, 437-453 (2015).
18. Ming, R., et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435-1442 (2015).
19. Cai, J., et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47, 65-72 (2015).
20. Hartwell, J., Dever, L. V. , Boxall, S. F. Emerging model systems for functional genomics analysis of crassulacean acid metabolism. Curr. Opin. Plant Biol. 31, 100-108 (2016).
21. Soltis, D. E., Soltis, P. S., Endress, P. K., & Chase, M. W. Phylogeny And Evolution Of Angiosperms. Sinauer Associates Inc. (2005).
22. Soltis, D. E., et al. Phylogenetic relationships and character evolution analysis of Saxifragales using a supermatrix approach. Am. J. Bot. 100, 916-929 (2013).
23. The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1-20 (2016).
24. Zeng, L., et al. Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets. New Phytol. 214, 1338-1354 (2017).
25. Moore, M. J., Soltis, P. S., Bell, C. D., Burleigh, J. G. , Soltis, D. E. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc. Natl Acad. Sci. USA 107, 4623-4628 (2010).
26. Maddison, W. P. , Knowles, L. L. Inferring phylogeny despite incomplete lineage sorting. Syst. Biol. 55, 21-30 (2006).
27. Degnan, J. H. , Rosenberg, N. A. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332-340 (2009).
28. Murat, F., et al. Karyotype and gene order evolution from reconstructed extinct ancestors highlight contrasts in genome plasticity of modern rosid crops. Genome Biol. Evol. 7, 735-749 (2015).
29. Jaillon, O., et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (2007).
30. Paterson, A. H., et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423-427 (2012).
31. Amborella Genome Project. The Amborella genome and the evolution of flowering plants. Science 342, 1241089 (2013).
32. Ledger, S., Strayer, C., Ashton, F., Kay, S. A. , Putterill, J. Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J. 26, 15-22 (2001).
33. Hsu, P. Y. , Harmer, S. L. Wheels within wheels: The plant circadian system. Trends Plant Sci. 19, 240-249 (2014).
34. Hartwell J. The Circadian Clock in CAM Plants. in Annual Plant Reviews: Endogenous Plant Rhythms (ed Hall A. J. W., McWatters H.). Blackwell Publishing (2006).
35. Hartwell, J., Nimmo, G., Wilkins, M., Jenkins, G. , Nimmo, H. Phosphoenolpyruvate carboxylase kinase is a novel protein kinase is a novel protein kinase regulated at the level of gene expression. Plant J. 20, 333-342 (1999).
36. Taybi, T., Patil, S., Chollet, R. , Cushman, J. A minimal Ser/Thr protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in CAMinduced leaves of Mesembryanthemum crystallinum. Plant Physiol. 123, 1471-1482 (2000).
37. Zhang, L., et al. Origin and mechanism of crassulacean acid metabolism in orchids as implied by comparative transcriptomics and genomics of the carbon fixation pathway. Plant J. 86, 175-185 (2016).
38. Schlieper, D., Förster, K., Paulus, J. K. , Groth, G. Resolving the activation site of positive regulators in plant phosphoenolpyruvate carboxylase. Mol. Plant 7, 437-440 (2014).
39. Nimmo, H. G. The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci. 5, 75-80 (2000).
40. Dever, L. V., Boxall, S. F., Kneová, 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. 167, 44-59 (2015).
41. Dittrich, P. Nicotinamide adenine dinucleotide-specific "malic" enzyme in Kalanchoë daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiol. 57, 310-314 (1976).
42. Kinoshita, T., et al. Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414, 656-660 (2001).
43. Krause, G. H., Winter, K., Krause, B. , Virgo, A. Protection by light against heat stress in leaves of tropical crassulacean acid metabolism plants containing high acid levels. Funct. Plant Biol. 43, 1061-1069 (2016).
44. Berry, J. , Björkman, O. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. 31, 491-543 (1980).
45. Salvucci, M. E. , Crafts-Brandner, S. J. Mechanism for deactivation of Rubisco under moderate heat stress. Physiol. Plant. 122, 513-519 (2004).
46. Wang, W., Vinocur, B., Shoseyov, O. , Altman, A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252 (2004).
47. Wang, G., et al. A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress. J. Exp. Bot. 66, 3027-3240 (2015).
48. Liu, C., et al. Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463, 197-202 (2010).
49. Nijhawan, A., Jain, M., Tyagi, A. K. , Khurana, J. P. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 146, 333-350 (2008).
50. Ram, H. , Chattopadhyay, S. Molecular interaction of bZIP domains of GBF1, HY5 and HYH in Arabidopsis seedling development. Plant Signal. Behav. 8, e22703 (2013).
51. Chen, X., et al. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26, 640-646 (2016).
52. Liu, D., Hu, R., Palla, K. J., Tuskan, G. A. , Yang, X. Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research. Curr. Opin. Plant Biol. 30, 70-77 (2016).
53. Borland, A. M., Guo, H.-B., Yang, X. , Cushman, J. C. Orchestration of carbohydrate processing for crassulacean acid metabolism. Curr. Opin. Plant Biol. 31, 118-124 (2016).
54. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. , Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495 (2014).
55. Yin, Y., et al. dbCAN: A web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40, W445-W451 (2012).
56. Martins, M. C. M., et al. Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol. 163, 1142-1163 (2013).
57. Xiang, L., et al. Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. J. Exp. Bot. 62, 3849-3862 (2011).
58. Sahm A., Bens M., Platzer M., Szafranski K. PosiGene: Automated and easy-touse pipeline for genome-wide detection of positively selected genes. Nucleic Acids Res. 45, e100, (2017).
59. Ito, N. , Phillips, S. E. Novel thioether bond revealed by a 1.7 A crystal structure of galactose oxidase. Nature 350, 87 (1991).
60. Black, C. C. , Osmond, C. B. Crassulacean acid metabolism photosynthesis: 'working the night shift'. Photosynth. Res. 76, 329-341 (2003).
61. De Paoli, H. C., Tuskan, G. A. , Yang, X. H. An innovative platform for quick and flexible joining of assorted DNA fragments. Sci. Rep. 6, 19278 (2016).
62. Wake, D. B., Wake, M. H. , Specht, C. D. Homoplasy: From detecting pattern to determining process and mechanism of evolution. Science 331, 1032-1035 (2011).
63. Laird, J. The law of parsimony. The Monist 29, 321-344 (1919).
64. Fujiki, Y., et al. Darkinducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol. Plant. 111, 345-352 (2001).
65. Puente, P., Wei, N. , Deng, X. W. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15, 3732 (1996).
66. Kajitani, R., et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res. 24, 1384-1395 (2014).
67. Bosi, E., et al. MeDuSa: A multi-draft based scaffolder. Bioinformatics 31, (2443-2451 (2015).
68. Enright, A. J., Van Dongen, S. , Ouzounis, C. A. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575-1584 (2002).
69. Gotz, S., et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420-3435 (2008).
70. Conesa, A., et al. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676 (2005).
71. Ekstrom, A., Taujale, R., McGinn, N. , Yin, Y. PlantCAZyme: A database for plant carbohydrate-active enzymes. Database (Oxford) 2014, bau079 (2014).
72. Kim, D., et al. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, 1 (2013).
73. Trapnell, C., et al. Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
74. Anders, S., Pyl, P. T. , Huber, W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
75. Mockler, T. C., et al. The Diurnal project: Diurnal and circadian expression profiling, model-based pattern matching, promoter analysis. Cold Spring Harb. Symp. Quant. Biol. 72, 353-363 (2007).
76. Roy, A., Kucukural, A. , Zhang, Y. I-TASSER: A unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738 (2010).
77. Yang, J., et al. The I-TASSER Suite: Protein structure and function prediction. Nat. Methods 12, 7-8 (2015).
78. Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).
79. Mirarab, S. , Warnow, T. ASTRAL-II: Coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44-i52 (2015).