Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Hori, Koichi ^a,b   Maruyama, Fumito ^c   Fujisawa, Takatomo ^d   Togashi, Tomoaki ^a   Yamamoto, Nozomi ^a   Seo, Mitsunori ^e   Sato, Syusei ^f   Yamada, Takuji ^a   Mori, Hiroshi ^a   Tajima, Naoyuki ^g   Moriyama, Takashi ^g   Ikeuchi, Masahiko ^g   Watanabe, Mai ^g   Wada, Hajime ^b,g   Kobayashi, Koichi ^g   Saito, Masakazu ^b,g   Masuda, Tatsuru ^g   Sasaki Sekimoto, Yuko ^a   Mashiguchi, Kiyoshi ^e   Awai, Koichiro ^h   Shimojima, Mie ^a   Masuda, Shinji ^a   Iwai, Masako ^a   Nobusawa, Takashi ^a,b   Narise, Takafumi ^a   Kondo, Satoshi ^a   Saito, Hikaru ^a   Sato, Ryoichi ^a   Murakawa, Masato ^a   Ihara, Yuta ^a   Oshima Yamada, Yui ^a   Ohtaka, Kinuka ^a   Satoh, Masanori ^a   Sonobe, Kohei ^a   Ishii, Midori ^a   Ohtani, Ryosuke ^a   Kanamori Sato, Miyu ^a   Honoki, Rina ^a   Miyazaki, Daichi ^a   Mochizuki, Hitoshi ^a   Umetsu, Jumpei ^a   Higashi, Kouichi ^a   Shibata, Daisuke ⁱ   Kamiya, Yuji ^e   Sato, Naoki ^b,g   Nakamura, Yasukazu ^d   Tabata, Satoshi ⁱ   Ida, Shigeru ^a   Kurokawa, Ken ^a,b   Ohta, Hiroyuki ^a,b   more..

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e RIKEN Center for Sustainable Resource Science   (Japan)

^f TOHOKU UNIVERSITY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h SHIZUOKA UNIVERSITY   (Japan)

ⁱ KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOHORMONE; CHLOROPHYLL;

ADAPTATION; ALGA; COLONIZATION; GENOME; HORMONE; LIGHT EFFECT; PLANT COMMUNITY; POPULATION GENETICS; TERRESTRIAL ECOSYSTEM;

ALGAL GENETICS; ARTICLE; CHAROPHYTA; EMBRYOPHYTA; EVOLUTIONARY ADAPTATION; HORMONE ACTION; KLEBSORMIDIUM FLACCIDUM; LIGHT INTENSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENETICS; PLANT GENOME; SIGNAL TRANSDUCTION; TERRESTRIAL SPECIES; VASCULAR PLANT; ADAPTATION; DNA SEQUENCE; ELECTRON TRANSPORT; FLUORESCENCE; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHASE CONTRAST MICROSCOPY; PHYLOGENY; PLANT GENE; PROTEIN TERTIARY STRUCTURE; STREPTOPHYTA;

ADAPTATION, PHYSIOLOGICAL; CHLOROPHYLL; ELECTRON TRANSPORT; FLUORESCENCE; GENES, PLANT; GENOME, PLANT; MASS SPECTROMETRY; MICROSCOPY, INTERFERENCE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PLANT GROWTH REGULATORS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; STREPTOPHYTA;

EID: 84901711172     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4978     Document Type: Article

References (60)

1. Parnell, J. & Foster, S. Ordovician ash geochemistry and the establishment of land plants. Geochem. Trans. 13, 7 (2012).
2. Scott, A. C. & Glasspool, I. J. The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. Proc. Natl Acad. Sci. USA 103, 10861-10865 (2006). (Pubitemid 44148386)
3. Lewis, L. A. & McCourt, R. M. Green algae and the origin of land plants. Am. J. Bot. 91, 1535-1556 (2004). (Pubitemid 43193718)
4. Leliaert, F. et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31, 1-46 (2012).
5. Timme, R. E., Bachvaroff, T. R. & Delwiche, C. F. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE 7, e29696 (2012).
6. Rensing, S. A. et al. The Physcomitrella Genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69 (2008).
7. Rindi, F. et al. Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta). Mol. Phylogenet. Evol. 58, 218-231 (2011).
8. Morison, M. O. & Sheath, R. G. Response to desiccation stress by Klebsormidium rivulare (Ulotrichales, Chlorophyta) from a Rhode Island stream. Phycologia 24, 129-145 (1985).
9. Elster, J. et al. Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63, 843-851 (2008).
10. Karsten, U. & Holzinger, A. Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microb. Ecol. 63, 51-63 (2012).
11. Nagao, M., Matsui, K. & Uemura, M. Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ. 31, 872-885 (2008). (Pubitemid 351667685)
12. Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 38, D211-D222 (2010).
13. Kersting, A. R., Bornberg-Bauer, E., Moore, A. D. & Grath, S. Dynamics and adaptive benefits of protein domain emergence and arrangements during plant genome evolution. Genome Biol. Evol. 4, 316-329 (2012).
14. Tarakhovskaya, E. R., Maslov, Y. I. & Shishova, M. F. Phytohormones in algae. Russ. J. Plant Physiol. 54, 163-170 (2007). (Pubitemid 46568941)
15. Le Bail, A. et al. Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol. 153, 128-144 (2010).
16. Niyogi, K. K. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 50, 333-359 (1999). (Pubitemid 129491966)
17. Muller, P., Li, X. & Niyogi, K. K. Non-photochemical quenching. a response to excess light energy. Plant Physiol. 125, 1558-1566 (2001). (Pubitemid 32375740)
18. Ifuku, K., Endo, T., Shikanai, T. & Aro, E.-M. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 52, 1560-1568 (2011).
19. Rumeau, D., Peltier, G. & Cournac, L. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30, 1041-1051 (2007). (Pubitemid 47179809)
20. Munekage, Y. et al. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361-371 (2002).
21. Mart́in, M. & Sabater, B. Plastid ndh genes in plant evolution. Plant Physiol. Biochem. 48, 636-645 (2010).
22. Shikanai, T. et al. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA 95, 9705-9709 (1998). (Pubitemid 28506296)
23. Hauser, F., Waadt, R. & Schroeder, J. I. Evolution of abscisic acid synthesis and signaling mechanisms. Curr. Biol. 21, R346-R355 (2011).
24. Santner, A. & Estelle, M. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071-1078 (2009).
25. Robert-Seilaniantz, A., Grant, M. & Jones, J. D. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev. Phytopathol. 49, 317-343 (2011).
26. Viaene, T., Delwiche, C. F., Rensing, S. A. & Friml, J. Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci. 18, 5-10 (2013).
27. Prochnik, S. E. et al. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329, 223-226 (2010).
28. Li, X. P. et al. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395 (2000).
29. Peers, G. et al. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518-521 (2009).
30. Gerotto, C. & Morosinotto, T. Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol. Plant 149, 583-598 (2013).
31. Collen, J. et al. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl Acad. Sci. USA. 110, 5247-5252 (2013).
32. Cock, J. M. et al. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465, 617-621 (2010).
33. Bowler, C. et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239-244 (2008).
34. Matsuzaki, M. et al. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428, 653-657 (2004). (Pubitemid 38524807)
35. Worden, A. Z. et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268-272 (2009).
36. Palenik, B. et al. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc. Natl Acad. Sci. USA 104, 7705-7710 (2007). (Pubitemid 47185970)
37. Blanc, G. et al. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22, 2943-2955 (2010).
38. Merchant, S. S. et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250 (2007).
39. Banks, J. A. et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963 (2011).
40. International rice genome sequencing project. The map-based sequence of the rice genome. Nature 436, 793-800 (2005).
41. Tuskan, G. A. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604 (2006). (Pubitemid 44414027)
42. Arabidopsis genome initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815 (2000).
43. Grigoriev, I. V. et al. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 40, D26-D32 (2012).
44. Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186 (2012).
45. Pruitt, K. D., Tatusova, T., Brown, G. R. & Maglott, D. R. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 40, D130-D135 (2012).
46. Altschul, S. F. et al. Basic local alignment search tool. J Mol Biol. 215, 403-410 (1990).
47. Li, L., Christian, J. S. & David, S. R. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003). (Pubitemid 37161775)
48. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002). (Pubitemid 34851225)
49. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
50. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004). (Pubitemid 38832724)
51. Talavera, G. & Castresana, J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564-577 (2007). (Pubitemid 47171631)
52. Tanabe, A. S. Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional, and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol. Ecol. Res. 11, 914-921 (2011).
53. Kumar, S., Stecher, G., Peterson, D. & Tamura, K. MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics 28, 2685-2686 (2012).
54. Santner, A., Calderon-Villalobos, L. I. & Estelle, M. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301-307 (2009).
55. Shi, J. H. & Yang, Z. B. Is ABP1 an auxin receptor yet? Mol. Plant 4, 635-640 (2011).
56. Fu, Z. Q. et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228-232 (2012)
57. Hall, T. A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser 41, 95-98 (1999).
58. Hofmann, K. & Stoffel, W. TMbase-a database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler 374, 166 (1993).
59. Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protien. J. Mol. Biol. 157, 105-132 (1982).
60. Yoshimoto, K. et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21, 2914-2927 (2009).