Abstract
Across the streptophyte lineage, which includes charophycean algae and embryophytic plants, there have been at least four independent transitions to the terrestrial habitat. One of these involved the evolution of embryophytes (bryophytes and tracheophytes) from a charophycean ancestor, while others involved the earliest branching lineages, containing the monotypic genera Mesostigma and Chlorokybus, and within the Klebsormidiales and Zygnematales lineages. To overcome heat, water stress, and increased exposure to ultraviolet radiation, which must have accompanied these transitions, adaptive mechanisms would have been required. During periods of dehydration and/or desiccation, proteomes struggle to maintain adequate cytoplasmic solute concentrations. The increased usage of charged amino acids (DEHKR) may be one way of maintaining protein hydration, while increased use of aromatic residues (FHWY) protects proteins and nucleic acids by absorbing damaging UV, with both groups of residues thought to be important for the stabilization of protein structures. To test these hypotheses we examined amino acid sequences of orthologous proteins representing both mitochondrion- and plastid-encoded proteomes across streptophytic lineages. We compared relative differences within categories of amino acid residues and found consistent patterns of amino acid compositional fluxuation in extra-membranous regions that correspond with episodes of terrestrialization: positive change in usage frequency for residues with charged side-chains, and aromatic residues of the light-capturing chloroplast proteomes. We also found a general decrease in the usage frequency of hydrophobic, aliphatic, and small residues. These results suggest that amino acid compositional shifts in extra-membrane regions of plastid and mitochondrial proteins may represent biochemical adaptations that allowed green plants to colonize the land.
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References
Banerjee T, Gupta SK, Ghosh TC (2006) Compositional transitions between Oryza sativa and Arabidopsis thaliana genes are linked to the functional change of encoded proteins. Plant Sci 170:267–273
Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004
Blum A, Ebercon A (1976) Genotypic responses in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Sci 16:428–431
Borders CL Jr, Broadwater JA, Bekeny PA, Salmon JE, Lee AS, Eldridge AM, Pett VB (1994) A structural role for arginine in proteins: multiple hydrogen bonds to backbone carbonyl oxygens. Protein Sci 3:541–548
Boussau B, Blanquart S, Necsulea A, Lartillot N, Gouy M (2008) Parallel adaptations to high temperatures in the Archaean eon. Nature 456:942–945
Brocchieri L (2004) Environmental signatures in proteome properties. Proc Natl Acad Sci USA 101:8257–8258
Brosche M, Strid A (2003) Molecular events following perception of ultraviolet- B radiation by plants. Physiol Plant 117:1–10
Bryant RG (1996) The dynamics of water-protein interactions. Annu Rev Biophys Biomol Struct 25:29–53
Carmo-Silva AE, Francisco A, Powers SJ, Keys AJ, Ascensão L, Parry MAJ, Arrabaça MC (2009) Grasses of different C4 subtypes reveal leaf traits related to drought tolerance in their natural habitats: changes in structure, water potential, and amino acid content. Am J Bot 96:1222–1235
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264
Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283
Close T (1997) A commonality in the response of plants to dehydration and low temperature. Physiol Plantarum 100:291–296
Cooper-Driver GA, Bhattacharya M (1998) Role of phenolics in plant evolution. Phytochemistry 49:1165–1174
Cruveiller S, Jabbari K, D’Onofrio G, Bernardi G (1999) Different hydrophobicities of orthologous proteins from Xenopus and human. Gene 238:15–21
Cuming AC (1999) LEA proteins. In: Shewry PR, Casey R (eds) Seed proteins. Kluwer, Netherlands, pp 753–780
de Bakker NV, van Bodegom PM, van de Poll WH, Boelen P, Nat E, Rozema J, Aerts R (2005) Is UV-B radiation affecting charophycean algae in shallow freshwater systems? New Phytol 166:957–966
Deckert G, Warren PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M, Huber R, Feldman RA, Short JM, Olsen GJ, Swanson RV (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392:353–358
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415
Foerstner KU, von Mering C, Hooper SD, Bork P (2005) Environments shape the nucleotide composition of genomes. EMBO Rep 6:1208–1213
Foster PG, Jermiin LS, Hickey DA (1997) Nucleotide composition bias affects amino acid content in proteins coded by animal mitochondria. J Mol Evol 44:282–288
Frank W, Ratnadewi D, Reski R (2005) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220:384–394
Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96:15324–15329
Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA 97:4535–4540
Granot G, Sikron-Persi N, Gaspan O, Florentin A, Talwara S, Paul LK, Morgenstern Y, Granot Y, Grafi G (2009) Histone modifications associated with drought tolerance in the desert plant Zygophyllum dumosum Boiss. Planta 231:27–34
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104
Gu X, Hewett-Emmett D, Li WH (1998) Directional mutational pressure affects the amino acid composition and hydrophobicity of proteins in bacteria. Genetica 102(103):383–391
Hájek T, Beckett RP (2008) Effect of water content components on desiccation and recovery in sphagnum mosses. Ann Bot 101:165–173
Haney PJ, Badger JH, Buldak GL, Reich CI, Woese CR, Olsen GJ (1999) Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. Proc Natl Acad Sci USA 96:3578–3583
Hanson DT, Swanson S, Graham LE, Sharkey TD (1999) Evolutionary significance of isoprene emission from mosses. Am J Bot 86:634–639
Ikehara K (2002) Origins of gene, genetic code, protein and life: comprehensive view of life systems from a GNC-SNS primitive genetic code hypothesis. J Biosci 27:165–186
Jabbari K, Cruveiller S, Clay O, Bernardi G (2003) The correlation between GC3 and hydropathy in human genes. Gene 317:137–140
Jaenicke R, Böhm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8:738–748
Jobson RW, Qiu YL (2008) Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct 3:43
Jobson RW, Dehne-Garcia A, Galtier N (2010) Apparent longevity-related adaptation of mitochondrial amino acid content is due to nucleotide compositional shifts. Mitochondrion 10:540–547
Kannan N, Vishveshwara S (2000) Aromatic clusters: a determinant of thermal stability of thermophilic proteins. Prot Eng 13:753–761
Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39
Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546
Killian JA, Heijne G (2000) How proteins adapt to a membrane-water interface. Trends Biochem Sci 25:429–434
King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798
Klotz IM (1958) Protein hydration and behavior. Science 128:815–822
Knight CG, Kassen R, Hebestreit H, Rainey PB (2004) Global analysis of predicted proteomes: functional adaptation of physical properties. Proc Natl Acad Sci USA 101:8390–8395
Kovács E, Keresztes A (2002) Effect of gamma and UV-B/C radiation on plant cells. Micron 33:199–203
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego
Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423
Kumar S, Nussinov R (2001) How do thermophilic proteins deal with heat? Cell Mol Life Sci 58:1216–1233
Lemieux C, Otis C, Turmel M (2007) A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5:2
Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556
Li L, Wang B, Liu Y, Qiu Y-L (2009) The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. J Mol Evol 68:665–678
Lobry JR, Chessel D (2003) Internal correspondence analysis of codon and amino-acid usage in thermophilic bacteria. J Appl Genet 44:235–261
McDonald JH (2001) Patterns of temperature adaptation in proteins from bacteria Deinococcus radiodurans and Thermus thermophilus. Mol Biol Evol 18:741–749
Mrabet NT, Van den Broeck A, Van den brande I, Stanssens P, Laroche Y, Lambeir AM, Matthijssens G, Jenkins J, Chiadmi M, van Tilbeurgh H et al (1992) Arginine residues as stabilizing elements in proteins. Biochemistry 31:2239–2253
Musto H, Naya H, Zavala A, Romero H, Alvarez-Valín F, Bernardi G (2004) Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Lett 573:73–77
Naya H, Romero H, Zavala A, Alvarez B, Musto H (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55:260–264
Nishio Y, Nakamura Y, Kawarabayasi Y, Usuda Y, Kimura E, Sugimoto S, Matsui K, Yamagishi A, Kikuchi H, Ikeo K, Gojobori T (2003) Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13:1572–1579
Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799
Popadin K, Polishchuk LV, Mamirova L, Knorre D, Gunbin K (2007) Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals. Proc Natl Acad Sci USA 104:13390–13395
Proctor MCF, Pence VC (2002) In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI, Wallingford, pp 207–237
Proctor MC, Smirnoff N (2000) Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. J Exp Bot 51:1695–1704
Proctor MC, Ligrone R, Duckett JG (2007) Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann Bot 99:75–93
Qiu Y-L (2008) Phylogeny and evolution of charophytic algae and land plants. J Syst Evol 46:287–306
Qiu Y-L, Palmer JD (1999) Phylogeny of early land plants: insights from genes and genomes. Trends Plant Sci 4:26–30
Qiu Y-L, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516
Qiu Y-L, Li L, Wang B, Chen Z, Dombrovska O, Lee J, Kent L, Li R, Jobson RW, Hendry TA, Taylor DW, Testa CM, Ambros M (2007) A non-flowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial and nuclear genes. Int J Plant Sci 168:691–708
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin-I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
Richardt S, Timmerhaus G, Lang D, Qudeimat E, Corrêa LG, Reski R, Rensing SA, Frank W (2010) Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol 72:27–45
Rodrigues GC, Jansen MAK, van den Noort ME, van Rensen JJS (2006) Evidence for the semireduced primary quinone electron acceptor of photosystem II being a photosensitizer for UVB damage to the photosynthetic apparatus. Plant Sci 170:283–290
Romero H, Pereira E, Naya H, Musto H (2009) Oxygen and guanine-cytosine profiles in marine environments. J Mol Evol 69:203–206
Saelensminde G, Halskau Ø Jr, Jonassen I (2009) Amino acid contacts in proteins adapted to different temperatures: hydrophobic interactions and surface charges play a key role. Extremophiles 3:11–20
Sanderson MJ (2004) Molecular evidence on plant divergence times. Am J Bot 91:1656–1665
Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101:5–18
Singer GA, Hickey DA (2003) Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317:39–47
Smith JC, Merzel F, Bondar AN, Tournier A, Fischer S (2004) Structure, dynamics and reactions of protein hydration water. Philos Trans R Soc Lond B Biol Sci 359:181–189
Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396
Strub C, Alies C, Lougarre A, Ladurantie C, Czaplicki J, Fournier D (2004) Mutation of exposed hydrophobic amino acids to arginine to increase protein stability. BMC Biochem 5:9
Tekaia F, Yeramian E (2006) Evolution of proteomes: fundamental signatures and global trends in amino acid compositions. BMC Genomics 7:307
Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338
Tyrrell RM (1994) The molecular and cellular pathology of solar ultraviolet radiation. Mol Asp Med 15:1–77
Wang HC, Singer GA, Hickey DA (2004) Mutational bias affects protein evolution in flowering plants. Mol Biol Evol 21:90–96
Wang B, Xue J-Y, Li L, Liu Y, Qiu Y-L (2009a) The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea reveals extremely conservative mitochondrial genome evolution in liverworts. Curr Genet 55:601–609
Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Pei ZM, Shen SH, He YK (2009b) Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiol 149:1739–1750
Waters ER (2003) Molecular adaptation and the origin of land plants. Mol Phylogenet Evol 29:456–463
Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97
Wolf L, Rizzini L, Stracke R, Ulm R, Rensing SA (2010) The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol 153:1123–1134
Xia X, Li W-H (1998) What amino acid properties affect protein evolution? J Mol Evol 47:557–564
Xue J-Y, Liu Y, Li L, Wang B, Qiu YL (2010) The complete mitochondrial genome sequence of the hornwort Phaeoceros laevis: retention of many ancient pseudogenes and conservative evolution of mitochondrial genomes in hornworts. Curr Genet 56:53–61
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We thank Jiayu Xue and Yang Liu for helpful contributions. This study was partly supported by NSF grant DEB 0531689 to Y.-L. Qiu.
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Jobson, R.W., Qiu, YL. Amino Acid Compositional Shifts During Streptophyte Transitions to Terrestrial Habitats. J Mol Evol 72, 204–214 (2011). https://doi.org/10.1007/s00239-010-9416-1
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DOI: https://doi.org/10.1007/s00239-010-9416-1