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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Comparative genomics of two ecologically differential populations of Hibiscus tiliaceus under salt stress

Guili Yang A , Xiaoshu Chen A , Tian Tang A , Renchao Zhou A , Sufang Chen A , Weijing Li A , Jianhua Ouyang A , Lian He A and Shuhua Shi A B
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Biocontrol, Key Laboratory of Gene Engineering of the Ministry of Education, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, Guangdong, The People’s Republic of China.

B Corresponding author. Email: lssssh@mail.sysu.edu.cn

Functional Plant Biology 38(3) 199-208 https://doi.org/10.1071/FP10228
Submitted: 24 November 2010  Accepted: 14 January 2011   Published: 29 March 2011

Abstract

Hibiscus tiliaceus L. is a mangrove associate that occupies the divergent environments of intertidal wetland (L population) and inland (T population). Thus, it is an ideal plant for the study of ecological adaptation and salt tolerance. In this study we compared responses of the two populations to salinity combining a global transcriptional analysis and physiological analysis. Microarray transcript profiling analysis showed both shared and divergent responses to salinity stress in the two populations. A total of 575 unigenes were identified as being salt-responsive in the two populations. Shared responses were exemplified by the regulated genes functioning in confining ribosomal functions, photosynthesis and cellular metabolism. A set of genes functioning in cellular transporting and cell detoxification and a crucial transcription factor AP2 domain-containing protein involved in environmental responsiveness, were differently expressed in the two populations. Physiological analysis showed that the L population was less susceptible to salt stress in photosynthesis and had a stronger capability of K+ : Na+ regulation than the T population. Both microarray and physiological data showed the L population possess higher fitness under high salinity, probably due to it its long-term adaptation to their native environment.

Additional keywords: adaptation, cDNA microarray, mangrove associate, salt stress.


References

Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Current Opinion in Biotechnology 13, 146–150.
Engineering salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1CltL8%3D&md5=751910c1a4c7c76c3462ae291c207ee1CAS | 11950567PubMed |

Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sju7s%3D&md5=100b7d568c0a92daa4d1ac981ff7c856CAS | 10455050PubMed |

Blumwald E (2000) Sodium transport and salt tolerance in plants. Current Opinion in Cell Biology 12, 431–434.
Sodium transport and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Srtbg%3D&md5=d1c0b6ba7b4401cb324c339a56e3e30fCAS | 10873827PubMed |

Bohnert HJ, Ayoubid P, Borcherta C, Bressan RA, Burnap RL (2001) A genomics approach towards salt stress tolerance. Plant Physiology and Biochemistry 39, 295–311.
A genomics approach towards salt stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFajsL4%3D&md5=61be98773dcd7951e2137dc30d4b8aa3CAS |

Carroll SB (2000) Endless forms: the evolution of gene regulation and morphological diversity. Cell 101, 577–580.
Endless forms: the evolution of gene regulation and morphological diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1Wrsbk%3D&md5=b2bc0458fa5d33013bef7c93f5341157CAS | 10892643PubMed |

Chen WJ, Chang SH, Hudson M, Kwan WK, Li J, Estes B, Knoll D, Shi L, Zhu T (2005) Contribution of transcriptional regulation to natural variations in Arabidopsis. Genome Biology 6, R32
Contribution of transcriptional regulation to natural variations in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15833119PubMed |

Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America 95, 14 863–14 868.
Cluster analysis and display of genome-wide expression patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVGmurk%3D&md5=6d7359ce2f1187bad10807b53e08c98fCAS |

Fu X, Huang Y, Deng S, Zhou R, Yang G, Ni X, Li W, Shi S (2005) Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Science 169, 147–154.
Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFegsLs%3D&md5=2bea827bb1b04efdfb97aac62d4ba3c2CAS |

Gibson G (2006) Evolution: the plastic transcriptorne. Current Biology 16, R285–R287.
Evolution: the plastic transcriptorne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvFWmur4%3D&md5=b9d10fb2c26d957087f60e35e9cb1ef1CAS | 16631573PubMed |

Gong Q, Li P, Ma S, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44, 826–839.
Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWltrbN&md5=e2c816f5aa50829f26d5e7de3b811878CAS | 16297073PubMed |

Harmer SL, Hogenesch JB, Straume M (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113.
Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVyisrw%3D&md5=f16671f63e90096bfa011a10da2efd55CAS | 11118138PubMed |

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=6cb239a13a0581221e65204097647e08CAS | 15012199PubMed |

Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. The Plant Journal 9, 537–548.
Coordinate transcriptional induction of myo-inositol metabolism during environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivFWntLk%3D&md5=c6fddd28f8b468e240c48c32e9f8d307CAS | 8624516PubMed |

Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. The Plant Cell 13, 889–905.

Kirch H-H, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends in Plant Science 9, 371–377.
The ALDH gene superfamily of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVCqtb8%3D&md5=d2a94094673c3b93b69adbdb8e93c4c6CAS | 15358267PubMed |

Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Molecular Ecology 15, 575–591.
Ecological and evolutionary genomics of Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVGnsL0%3D&md5=cd51d669f2b7643f74153a53d26d8d9bCAS | 16499686PubMed |

Larsen PF, Nielsen EE, Williams T, Hemmer-Hansen J, Chipman JK (2007) Adaptive differences in gene expression in European flounder (Platichthys flesus). Molecular Ecology 16, 4674–4683.
Adaptive differences in gene expression in European flounder (Platichthys flesus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFahtQ%3D%3D&md5=ed0f3f0f24f37783f3f00575cbeae562CAS | 17922814PubMed |

Lee EC, Mitchell-Olds T (2006) Preface to the special issue: ecological and evolutionary genomics of populations in nature. Molecular Ecology 15, 1193–1196.
Preface to the special issue: ecological and evolutionary genomics of populations in nature.Crossref | GoogleScholarGoogle Scholar | 16626447PubMed |

Levine M, Tjian R (2003) Transcription regulation and animal diversity. Nature 424, 147–151.
Transcription regulation and animal diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlt1CktLw%3D&md5=787d5b808d9e0d30f41f76ce22fcc321CAS | 12853946PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=fb7f5980d7bf4d62f797a1988cd8f193CAS | 11846609PubMed |

Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios. Annals of Botany 84, 123–133.
K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCgtL4%3D&md5=6a8b3acc292f331f42fa2dc461ee591aCAS |

Miyama M, Shimizu H, Sugiyama M, Hanagata N (2006) Sequencing and analysis of 14,842 expressed sequence tags of Burma mangrove, Bruguiera gymnorrhiza. Plant Science 171, 234–241.
Sequencing and analysis of 14,842 expressed sequence tags of Burma mangrove, Bruguiera gymnorrhiza.Crossref | GoogleScholarGoogle Scholar |

Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nature Genetics 32, 261–266.
Variation in gene expression within and among natural populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlaisLo%3D&md5=eb0305b8632765151df5c844a8b155dcCAS | 12219088PubMed |

Ouborg NJ, Vriezen WH (2007) An ecologist’s guide to ecogenomics. Journal of Ecology 95, 8–16.
An ecologist’s guide to ecogenomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1aju70%3D&md5=f739bf9ea5ec9e773527e6726b739cfbCAS |

Popp M, Larher F, Weigel P (1985) Osmotic adaptation in Australia mangroves. Plant Ecology 61, 247–253.
Osmotic adaptation in Australia mangroves.Crossref | GoogleScholarGoogle Scholar |

Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics 37, 1141–1146.
A rice quantitative trait locus for salt tolerance encodes a sodium transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCntL%2FJ&md5=5784135a3ff4398ada7a0a96c5ee78e3CAS | 16155566PubMed |

Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Ulrich G, Gertrud M, Musterkotter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Research 32, 5539–5545.
The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVOiu74%3D&md5=019e77bf9516ff25a3cb709b116f80b8CAS | 15486203PubMed |

Santiago LS, Lau TL, Melcher PJ, Steele OC, Goldstein G (2000) Morphological and physiological responses of Hawaiian Hibiscus tiliaceus populations to light and salinity. International Journal of Plant Sciences 161, 99–106.
Morphological and physiological responses of Hawaiian Hibiscus tiliaceus populations to light and salinity.Crossref | GoogleScholarGoogle Scholar | 10648199PubMed |

Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian regulated genes in Arabidopsis. The Plant Cell 13, 113–123.

Serrano R, Mulet J, Rios G, Marquez J, Larrinoa I, Leube M (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. Journal of Experimental Botany 50, 1023–1036.
A glimpse of the mechanisms of ion homeostasis during salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVehsrc%3D&md5=efd33bc8574766a5261da011ab1925a4CAS |

Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeaty DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences of the United States of America 94, 1035–1040.
Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeaty DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtVyhsLc%3D&md5=8ad4a9e3de7fbb7f119ebb63a7eb2ad4CAS | 9023378PubMed |

Stone JR, Wray GA (2001) Rapid evolution of cis-regulatory sequences via local point mutations. Molecular Biology and Evolution 18, 1764–1770.

Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiology 135, 1697–1709.
Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqsb4%3D&md5=ee7632e4deacde5d0295dd90c1189fc0CAS | 15247402PubMed |

Tang T, Zhong Y, Jian S, Shi S (2003) Genetic diversity of Hibiscus tiliaceus (Malvaceae) in China. Annals of Botany 92, 409–414.
Genetic diversity of Hibiscus tiliaceus (Malvaceae) in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVShsLs%3D&md5=cd94e3b442912ec4e7bf424e77db1888CAS | 12930729PubMed |

Tomlinson PB (1986) ‘The botany of mangroves.’ (Cambridge University Press: Cambridge)

Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 98, 5116–5121.
Significance analysis of microarrays applied to the ionizing radiation response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1Ons7w%3D&md5=c0a2450bc288345ee0e10feb036bd176CAS | 11309499PubMed |

Wang H, Miyazaki S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Molecular Biology 52, 873–891.
Temporal progression of gene expression responses to salt shock in maize roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVenur8%3D&md5=8778211f26a8d22bc0c84f9d02242b3bCAS | 13677474PubMed |

Whitehead A, Crawford DL (2006) Variation within and among species in gene expression: raw material for evolution. Molecular Ecology 15, 1197–1211.
Variation within and among species in gene expression: raw material for evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvFyls7c%3D&md5=1531d563751f38b4cbbb52b40b9ab87bCAS | 16626448PubMed |

Yang G, Zhou R, Tang T, Shi S (2008) Simple and efficient isolation of high-quality total RNA from Hibiscus tiliaceus, a mangrove associate and its relatives. Preparative Biochemistry & Biotechnology 38, 257–264.
Simple and efficient isolation of high-quality total RNA from Hibiscus tiliaceus, a mangrove associate and its relatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVCgsrg%3D&md5=afff343f1feefaf9d8f035e5e7d58924CAS | 18569872PubMed |

Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). The Plant Journal 42, 689–707.
Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1yns7w%3D&md5=63432b6647194538e1667f6b7e4d2b8bCAS | 15918883PubMed |

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyjtLs%3D&md5=afaf72ccbc5aaac06af37bb8b6ef97b6CAS | 11173290PubMed |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbc%3D&md5=6fad0f73ea8700fb8a10c3992bf11d79CAS | 12221975PubMed |