Sciences in Cold and Arid Regions ›› 2017, Vol. 9 ›› Issue (1): 78–88.doi: 10.3724/SP.J.1226.2017.00078

• • 上一篇    

Adaptive evolution of rbcL in Reaumuria soongarica (Tamaricaceae)

ChaoJu Qian1,2, MengHe Gu3, HengXia Yin1,2, Yong Shi1,2, ChengLiang Yin1,2, Xia Yan1,4, XiaoFei Ma1   

  1. 1. Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions, Gansu Province, Department of Ecology and Agriculture Research, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China;
    2. University of Chinese Academy of Sciences, Beijing 100049, China;
    3. Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China;
    4. Key Laboratory of Eco-hydrology and of Inland River Basin, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
  • 收稿日期:2016-08-30 修回日期:2016-11-12 发布日期:2018-11-23
  • 通讯作者: Xia Yan, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. E-mail:yanxia@lzb.ac.cn E-mail:Xia Yan, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. E-mail:yanxia@lzb.ac.cn
  • 基金资助:
    This work was supported by the National Natural Science Foundation of China (NSFC, Grant Nos. 31370395 and 31500266) and the "One Hundred Tal-ents" project of the Chinese Academy of Sciences (Grant No. 29Y127E71).

Adaptive evolution of rbcL in Reaumuria soongarica (Tamaricaceae)

ChaoJu Qian1,2, MengHe Gu3, HengXia Yin1,2, Yong Shi1,2, ChengLiang Yin1,2, Xia Yan1,4, XiaoFei Ma1   

  1. 1. Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions, Gansu Province, Department of Ecology and Agriculture Research, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China;
    2. University of Chinese Academy of Sciences, Beijing 100049, China;
    3. Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China;
    4. Key Laboratory of Eco-hydrology and of Inland River Basin, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
  • Received:2016-08-30 Revised:2016-11-12 Published:2018-11-23
  • Contact: Xia Yan, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. E-mail:yanxia@lzb.ac.cn E-mail:Xia Yan, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. E-mail:yanxia@lzb.ac.cn
  • Supported by:
    This work was supported by the National Natural Science Foundation of China (NSFC, Grant Nos. 31370395 and 31500266) and the "One Hundred Tal-ents" project of the Chinese Academy of Sciences (Grant No. 29Y127E71).

摘要: In the field of phylogenetic analyses, the rbcL gene encoded large subunit Ribulose-1,5-biphosphate carboxylase/oxygenase (Rubisco, EC4.1.1.39), which plays a crucial role in the process of photosynthesis for most terrestrial plants, has been considered to be conserved; however, recent controversy regarding rbcL conservation has appeared since it was proposed to be under natural selection within all principal lineages of land plants. In this study, by examining the variation of DNA and protein sequences among 17 species in the family Tamaricaceae, three nonsynonymous mutations were identified to be under positive selection. The favored sites were located in the alph-helix domains of Rubisco, with decreased hydrophobicity and increased entropy, which could facilitate CO2 penetration into the active site of Rubisco. We also found that the expression level of rbcL in different genotypes of Reaumuria soongarica shifted in response to various stresses such as drought, temperature, salt, and light. This study not only sheds light on the functional/structural features of Rubisco in the evolution scenarios from C3-like into C4 in Tamaricaceae but also provides useful information on directing genetic performance to enhance photosynthesis efficiency of desert plants for sustaining fragile desert ecosystems; furthermore, it promotes the ability to cope with desert aridification and global warming.

关键词: rbcL gene, Reaumuria soongarica, Tamaricaceae, adaptive evolution

Abstract: In the field of phylogenetic analyses, the rbcL gene encoded large subunit Ribulose-1,5-biphosphate carboxylase/oxygenase (Rubisco, EC4.1.1.39), which plays a crucial role in the process of photosynthesis for most terrestrial plants, has been considered to be conserved; however, recent controversy regarding rbcL conservation has appeared since it was proposed to be under natural selection within all principal lineages of land plants. In this study, by examining the variation of DNA and protein sequences among 17 species in the family Tamaricaceae, three nonsynonymous mutations were identified to be under positive selection. The favored sites were located in the alph-helix domains of Rubisco, with decreased hydrophobicity and increased entropy, which could facilitate CO2 penetration into the active site of Rubisco. We also found that the expression level of rbcL in different genotypes of Reaumuria soongarica shifted in response to various stresses such as drought, temperature, salt, and light. This study not only sheds light on the functional/structural features of Rubisco in the evolution scenarios from C3-like into C4 in Tamaricaceae but also provides useful information on directing genetic performance to enhance photosynthesis efficiency of desert plants for sustaining fragile desert ecosystems; furthermore, it promotes the ability to cope with desert aridification and global warming.

Key words: rbcL gene, Reaumuria soongarica, Tamaricaceae, adaptive evolution

Akaike H, 1974. A new look at the statistical model identification. Automatic Control, IEEE Transactions, 19:716-723.
Barhoumi Z, Djebali W, Chaibi W, et al., 2007. Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. Journal of Plant Research, 120(4):529-537.
Bausher MG, Singh ND, Lee SB, et al., 2006. The complete chlo-roplast genome sequence of Citrus sinensis (L.) Osbeck var Ridge Pineapple:organization and phylogenetic relationships to other angiosperms. BMC Plant Biology, 6:21.
Bchini H, Ben Naceur M, Sayar R, et al., 2010. Genotypic differ-ences in root and shoot growth of barley (Hordeum vulgare L.) grown under different salinity levels. Hereditas, 147(3):114-122.
Bowman SM, Patel M, Yerramsetty P, et al., 2013. A novel RNA binding protein affects rbcL gene expression and is specific to bundle sheath chloroplasts in C4 plants. BMC Plant Biology, 13:138.
Brautigam A, Kajala K, Wullenweber J, et al., 2011. An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiology, 155(1):142-156.
Carmo-Silva AE, Keys AJ, Andralojc PJ, et al., 2010. Rubisco activities, properties, and regulation in three different C4 grasses under drought. Journal of Experimental Botany, 61(9):2355-2366.
Carmo-Silva AE, Salvucci ME, 2012. The temperature response of CO2 assimilation, photochemical activities and Rubisco acti-vation in Camelina sativa, a potential bioenergy crop with lim-ited capacity for acclimation to heat stress. Planta, 236(5):1433-1445.
Chase MW, Soltis DE, Olmstead RG, et al., 1993. Phylogenetics of seed plants:an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden, 80(3):528-580.
Christin PA, Osborne CP, 2013. The recurrent assembly of C4 photosynthesis, an evolutionary tale. Photosynthesis Research, 117(1-3):163-175.
Christin PA, Salamin N, Muasya AM, et al., 2008. Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis. Molecular Biology and Evolution, 25(11):2361-2368.
Delgado E, Medrano H, Keys AJ, et al., 1995. Species variation in Rubisco specificity factor. Journal of Experimental Botany, 46(292):1775-1777.
Du QJ, Dai KR, Li JM, et al., 2015. Effects of sub-low temperature and drought stress on characteristics of photosynthetic and fluorescence kinetics in tomato leaves. The Journal of Applied Ecology, 26(6):1687-1694.
Fu H, Yuan G, Zhong J, et al., 2013. Environmental and ontogenetic effects on intraspecific trait variation of a macrophyte species across five ecological scales. PLoS ONE, 8(4):e62794.
Galmes J, Aranjuelo I, Medrano H, et al., 2013. Variation in Ru-bisco content and activity under variable climatic factors. Photosynthesis Research, 117(1-3):73-90.
Galmes J, Flexas J, Keys A, et al., 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell and Environment, 28:9.
Galmés J, Flexas J, Keys AJ, et al., 2005. Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell & Environment, 28:571-579.
Galmes J, Kapralov MV, Copolovici LO, et al., 2015. Temperature responses of the Rubisco maximum carboxylase activity across domains of life:phylogenetic signals, trade-offs, and im-portance for carbon gain. Photosynthesis Research, 123(2):183-201.
Gould SJ, Lewontin RC, 1979. The spandrels of San Marco and the Panglossian paradigm:a critique of the adaptationist pro-gramme. Proceedings of the Royal Society of London B:Bio-logical Sciences, 205:581-598.
Guindon S, Gascuel O, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52:696-704.
Guo SJ, Yang KM, Huo J, et al., 2015. Influence of drought on leaf photosynthetic capacity and root growth of soybeans at grain filling stage. The Journal of Applied Ecology, 26(5):1419-1425.
Hall TA, 1999. BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.
Hou X, 1987. Geographical distribution of vegetation in arid desert area of Chinese temperate zones. Botany Bulletin, (2):37-66.
Hozain MI, Salvucci ME, Fokar M, et al., 2010. The differential response of photosynthesis to high temperature for a boreal and temperate Populus species relates to differences in Rubisco activation and Rubisco activase properties. Tree Physiology, 30(1):32-44.
Huang Y, Wang X, Ge S, et al., 2015. Divergence and adaptive evolution of the gibberellin oxidase genes in plants. BMC Evolutionary Biology, 15(1):1-15.
Iida S, Miyagi A, Aoki S, et al., 2009. Molecular adaptation of rbcL in the heterophyllous aquatic plant Potamogeton. PLoS ONE, 4(2):e4633.
Johnson LC, Olsen JT, Tetreault H, et al., 2015. Intraspecific variation of a dominant grass and local adaptation in reciprocal garden communities along a US Great Plains' precipitation gradient:implications for grassland restoration with climate change. Evolutionary Applications, 8(7):705-723.
Jordan DB, Ogren WL, 1981. Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature, 291(5815):513-515.
Kapralov MV, Filatov DA, 2006. Molecular adaptation during adaptive radiation in the Hawaiian endemic genus Schiedea. PLoS ONE, 1:e8.
Kapralov MV, Kubien DS, Andersson I, et al., 2011. Changes in Rubisco kinetics during the evolution of C4 photosynthesis in Flaveria (Asteraceae) are associated with positive selection on genes encoding the enzyme. Molecular Biology and Evolution, 28(4):1491-1503.
Keane T, Naughton T, McInerney J, 2004. ModelGenerator:amino acid and nucleotide substitution model selection. National University of Ireland, Maynooth, Ireland, 34.
Kubien DS, Whitney SM, Moore PV, et al., 2008. The biochemistry of Rubisco in Flaveria. Journal of Experimental Botany, 59(7):1767-1777.
Leebens-Mack J, DePamphilis C, 2002. Power analysis of tests for loss of selective constraint in cave crayfish and nonphotosyn-thetic plant lineages. Molecular Biology and Evolution, 19(8):1292-1302.
Li ZH, Chen J, Zhao GF, et al., 2012. Response of a desert shrub to past geological and climatic change:A phylogeographic study of Reaumuria soongarica (Tamaricaceae) in western China. Journal of Systematics and Evolution, 50(4):351-361.
Liu Q, Zhu Z, 2010. Functional divergence of the NIP III subgroup proteins involved altered selective constraints and positive se-lection. BMC Plant Biology, 10(1):1-12.
Lowry DB, Hall MC, Salt DE, et al., 2009. Genetic and physio-logical basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. The New Phytologist, 183(3):776-788.
Ma JY, Chen K, Xia DS, et al., 2007. Variation in foliar stable carbon isotope among populations of a desert plant, Reaumuria soongorica (Pall.) Maxim. in different environments. Journal of Arid Environments, 69(3):365-374.
Mehrotra S, Trivedi PK, Sethuraman A, et al., 2011. The rbcL gene of Populus deltoides has multiple transcripts and is re-dox-regulated in vitro. Journal of Plant Physiology, 168(5):466-473.
Miwa H, Odrzykoski IJ, Matsui A, et al., 2009. Adaptive evolution of rbcL in Conocephalum (Hepaticae, bryophytes). Gene, 441(1-2):169-175.
Mori S, Castoreno A, Lammers PJ, 2002. Transcript levels of rbcR1, ntcA, and rbcL/S genes in cyanobacterium Anabaena sp. PCC 7120 are downregulated in response to cold and osmotic stress. FEMS Microbiology Letters, 213(2):167-173.
Nishimura K, Ogawa T, Ashida H, et al., 2008. Molecular mecha-nisms of Rubisco biosynthesis in higher plants. Plant Biotech-nology, 25(3):285-290.
Parry MA, Andralojc PJ, Khan S, et al., 2002. Rubisco activity:effects of drought stress. Annals of Botany, 89(Spec.):833-839.
Petit JR, Jouzel J, Raynaud D, et al., 1999. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature, 399(6735):429-436.
Randle CP, Wolfe AD, 2005. The evolution and expression of RBCL in holoparasitic sister-genera Harveya and Hyobanche (Orobanchaceae). American Journal of Botany, 92(9):1575-1585.
Savir Y, Noor E, Milo R, et al., 2010. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. Proceedings of the National Academy of Sciences of the United States of America, 107(8):3475-3480.
Schrodinger LLC, 2010. The AxPyMOL Molecular Graphics Plugin for Microsoft PowerPoint, Version 1.0.
Sen L, Fares MA, Liang B, et al., 2011. Molecular evolution of rbcL in three gymnosperm families:identifying adaptive and coevolutionary patterns. Biology Direct, 6:29.
Sharkey TD, Seemann JR, 1989. Mild water stress effects on carbon-reduction-cycle intermediates, ribulose bisphosphate carboxylase activity, and spatial homogeneity of photosynthesis in intact leaves. Plant physiology, 89(4):1060-1065.
Shi Y, Yan X, Zhao P, et al., 2013. Transcriptomic analysis of a tertiary relict plant, extreme xerophyte Reaumuria soongorica to identify genes related to drought adaptation. PLoS ONE, 8(5):e63993.
Strauss SH, Palmer JD, Howe GT, et al., 1988. Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proceedings of the National Academy of Sciences, 85(11):3898-3902.
Sun H, Guo K, Feng S, et al., 2015. Positive selection drives adaptive diversification of the 4-coumarate:CoA ligase (4CL) gene in angiosperms. Ecology and Evolution, 5(16):3413-3420.
Tcherkez GG, Farquhar GD, Andrews TJ, 2006. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences of the United States of America, 103(19):7246-7251.
Ueno O, 1998. Induction of kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. The Plant Cell, 10(4):571-584.
Wang G, Kong F, Zhang S, et al., 2015. A tomato chloro-plast-targeted DnaJ protein protects Rubisco activity under heat stress. Journal of Experimental Botany, 66(11):3027-3040.
Wang M, Kapralov M, Anisimova M, 2011. Coevolution of amino acid residues in the key photosynthetic enzyme Rubisco. BMC Evolutionary Biology, 11(1):266.
Williams BP, Aubry S, Hibberd JM, 2012. Molecular evolution of genes recruited into C4 photosynthesis. Trends in Plant Science, 17(4):213-220.
Wolfe AD, dePamphilis CW, 1997. Alternate paths of evolution for the photosynthetic gene rbcL in four nonphotosynthetic species of Orobanche. Plant Molecular Biology, 33(6):965-977.
Wolfe AD, dePamphilis CW, 1998. The effect of relaxed functional constraints on the photosynthetic gene rbcL in photosynthetic and nonphotosynthetic parasitic plants. Molecular Biology and Evolution, 15(10):1243-1258.
Yan X, Dong X, Zhang W, et al., 2014. Reference gene selection for quantitative real-time PCR normalization in Reaumuria soon-gorica. PLoS ONE, 9(8):e104124.
Yang Z, 2007. PAML 4:phylogenetic analysis by maximum like-lihood. Molecular Biology and Evolution, 24(8):1586-1591.
Yin H, Yan X, Shi Y, et al., 2015. The role of East Asian monsoon system in shaping population divergence and dynamics of a constructive desert shrub Reaumuria soongarica. Scientific Reports, 5:15823.
Young JN, Rickaby RE, Kapralov MV, et al., 2012. Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide. Philosophical transactions of the Royal Society of London (Series B:Biological Sciences), 367(1588):483-492.
Zachos J, Pagani M, Sloan L, et al., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292(5517):686-693.
Zhang JY, Chen JX C, 2010. Salinity tolerance and genetic diversity of the dinoflagllate Oxyrrhis marina. Journal of Ocean Uni-versity of China, 9(1):87-93.
Zhao Z, Liu H, Luo Y, et al., 2014. Molecular evolution and functional divergence of tubulin superfamily in the fungal tree of life. Scientific Reports, 4:6746.
Zhou SX, Medlyn BE, Prentice IC, 2015. Long-term water stress leads to acclimation of drought sensitivity of photosynthetic capacity in xeric but not riparian Eucalyptus species. Annals of Botany, 117(1):133-144.
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