Expression of maize heat shock transcription factor gene ZmHsf06 enhances the thermotolerance and drought-stress tolerance of transgenic Arabidopsis
Hui-cong Li A , Hua-ning Zhang A , Guo-liang Li A B , Zi-hui Liu A , Yan-min Zhang A , Hong-mei Zhang A and Xiu-lin Guo A BA Plant Genetic Engineering Center of Hebei Province/Institute of Genetics and Physiology, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang 050051, PR China.
B Corresponding authors. Emails: myhf2002@163.com; guolianglili@163.com
Functional Plant Biology 42(11) 1080-1091 https://doi.org/10.1071/FP15080
Submitted: 30 March 2015 Accepted: 4 September 2015 Published: 28 September 2015
Abstract
Based on the information of 25 heat shock transcription factor (Hsf) homologues in maize according to a genome-wide analysis, ZmHsf06 was cloned from maize leaves and transformed into Arabidopsis thaliana (L. Heynh.) (ecotype, Col-0). Three transgenic positive lines were selected to assess the basic and acquired thermotolerance and drought-stress tolerance under stresses and for some physiological assays. The sequence analysis indicates that ZmHsf06 contained the characteristic domains of class A type plant Hsfs. The results of qRT–PCR showed that the expression levels of ZmHsf06 were elevated by heat shock and drought stress to different extents in three transgenic lines. Phenotypic observation shows that compared with the Wt (wild-type) controls, the overexpressing ZmHsf06 of Arabidopsis plants have enhanced basal and acquired thermotolerance, stronger drought-stress tolerance and growth advantages under mild heat stress conditions. These results are further confirmed by physiological and biochemical evidence that transgenic Arabidopsis plants exhibit higher seed germination rate, longer axial-root length, higher activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT), higher leaf chlorophyll content, but lower relative electrical conductivity (REC), malondialdehyde (MDA) and osmotic potential (OP) than the Wt controls after heat shock and drought treatments. ZmHsf06 may be a central representative of maize Hsfs and could be useful in molecular breeding of maize or other crops for enhanced tolerances, particularly during terminal heat and drought stresses.
Additional keywords: drought-stress tolerance, heat shock transcription factor, transformation, thermotolerance, ZmHsf06.
References
Agashe VR, Hartl FU (2000) Roles of molecular chaperones in cytoplasmic protein folding. Seminars in Cell & Developmental Biology 11, 15–25.| Roles of molecular chaperones in cytoplasmic protein folding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivF2murY%3D&md5=c9d2a5938de645fc66eb331a7d4ecb2aCAS |
Almoguera C, Rojas A, Díaz-Martín J, Prieto-Dapena P, Carranco R (2002) A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. Journal of Biological Chemistry 277, 43866–43872.
| A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1aksro%3D&md5=68ff4fbbab52cb7cd4a4ed8d892cba91CAS | 12228226PubMed |
Aranda MA, Escaler M, Thomas CL, Maule AJ (1999) A heat shock transcription factor in pea is differentially controlled by heat and virus replication. The Plant Journal 20, 153–161.
| A heat shock transcription factor in pea is differentially controlled by heat and virus replication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFait78%3D&md5=918a126fa60f14cbebcb8ed879eab3c0CAS | 10571875PubMed |
Baniwal SK, Bhaerti K, Chan KY, Fauth M, Ganguli A (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. Journal of Biosciences 29, 471–487.
| Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFWrurg%3D&md5=3100e8f67288a9afba4eca3c543a094dCAS | 15625403PubMed |
Busch W, Wunderlich M, Schöffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. The Plant Journal 14, 1–14.
Charng YY, Liu HC, Liu NY, Chi WT, Wang CN (2007) A heat-induced transcription factor, HSFA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiology 143, 251–262.
| A heat-induced transcription factor, HSFA2, is required for extension of acquired thermotolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1OntQ%3D%3D&md5=2e9fe8723c690540dbaa86c6c60c41f7CAS | 17085506PubMed |
Chauhan H, Khurana N, Agarwal P, Khurana JP, Khurana P (2013) A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. PLoS One 8, e79577
| A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsl2jtbrJ&md5=cd68ac66d566482d7194a323d4c5513bCAS | 24265778PubMed |
Clough Sj, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7mvVagsQ%3D%3D&md5=741485fe2409a913fdc44badd7788eeaCAS | 10069079PubMed |
Czarnecka-Verner E, Yuan CX, Fox PC, Gurley WB (1995) Isolation and characterization of six heat shock transcription factor cDNA clones from soybean. Plant Molecular Biology 29, 37–51.
| Isolation and characterization of six heat shock transcription factor cDNA clones from soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovVeksL8%3D&md5=932ac3db85499d11f391cf15a6a07c84CAS | 7579166PubMed |
Ellis RJ (2000) Chaperone substrates inside the cell. Trends in Biochemical Sciences 25, 210–212.
| Chaperone substrates inside the cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVeru74%3D&md5=a895c64c579d935911e8b2aa6de3086dCAS | 10782086PubMed |
Gagliardi D, Breton C, Chaboud A, Vergne P, Dumas C (1995) Expression of heat shock factor and heat shock protein 70 genes during maize pollen development. Plant Molecular Biology 29, 841–856.
| Expression of heat shock factor and heat shock protein 70 genes during maize pollen development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitF2mug%3D%3D&md5=f96df6c726b28bd53f81f4b7720087b5CAS | 8541509PubMed |
Guo JK, Wu J, Ji Q, Wang C, Luo L (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. Journal of Genetics and Genomics 35, 105–118.
| Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1ars7g%3D&md5=caa64fe1bdae5ee9c3238b7fd5119a30CAS |
Hayhoe K, Cayan D, Field CB, Frumhoff P, Maurer E (2004) Emissions pathways, climate change, and impacts on California. Proceedings of the National Academy of Sciences of the United States of America 101, 12422–12427.
| Emissions pathways, climate change, and impacts on California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVensrY%3D&md5=263d4ce30345671110bc5c29402fe7b8CAS | 15314227PubMed |
He P, Osaki M, Takebe M, Shinano T (2002) Changes of photosynthetic characteristics in relation to leaf senescence in two maize hybrids with different senescent appearance. Photosynthetica 40, 547–552.
| Changes of photosynthetic characteristics in relation to leaf senescence in two maize hybrids with different senescent appearance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1Okt74%3D&md5=eecd8625e826beea30e83f34abe9e5edCAS |
Heerklotz D, Döring P, Bonzelius F, Winkelhaus S, Nover L (2001) The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HSFA2. Molecular and Cellular Biology 21, 1759–1768.
| The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HSFA2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlGhsbs%3D&md5=3b3e5d0245daa86236fdcc8b0ca4224cCAS | 11238913PubMed |
Hübel A, Schöffl F (1994) Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein. Plant Molecular Biology 26, 353–362.
| Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein.Crossref | GoogleScholarGoogle Scholar | 7948881PubMed |
Jolly C, Morimoto RI (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. Journal of the National Cancer Institute 92, 1564–1572.
| Role of the heat shock response and molecular chaperones in oncogenesis and cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVKitr4%3D&md5=52d0659c528a42d20190a8a4f1e7c6f3CAS | 11018092PubMed |
Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiology 138, 882–897.
| Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVejs74%3D&md5=d47405cdaeb8c6926d9f23975ac9f1daCAS | 15923322PubMed |
Lee JH, Hübel A, Schöffl F (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. The Plant Journal 8, 603–612.
| Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpslSnu7s%3D&md5=41a548f9d988d3bddc75ec452f05c5aaCAS | 7496404PubMed |
Li HS (1999) ‘Principle and technique in plant physiology and biochemistry.’ (Higher Education Press: Beijing) [in Chinese]
Li HC, Li GL, Liu ZH, Zhang HM, Zhang YM (2014a) Cloning, localization and expression of ZmHSF-Like in Zea mays. Journal of Integrative Agriculture 13, 1230–1238.
| Cloning, localization and expression of ZmHSF-Like in Zea mays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtF2qsL4%3D&md5=d8e5f5a33ab499a43d8f6ec164776c1eCAS |
Li PS, Yu TF, He GH, Chen M, Zhou YB, Chai SC, Xu ZS, Ma YZ (2014b) Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement of drought and heat stresses. BMC Genomics 15, 1009
| Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement of drought and heat stresses.Crossref | GoogleScholarGoogle Scholar | 25416131PubMed |
Li HC, Li GL, Guo XL (2015) Cloning, expression characteristics and subcellular-location of heat shock transcription factor ZmHsf06 in Zea mays. Journal of Agricultural Biotechnology 23, 41–51. [in Chinese]
Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12, 76–89.
| Genome-wide identification, classification and analysis of heat shock transcription factor family in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVKmtLw%3D&md5=a5db1a6592d5bebd1bb9e5a8cbc53989CAS | 21272351PubMed |
Liu GR, Chen XZ, Duan WQ (2002) The relationship between wheat leaf osmotic adjustment ability and varietal drought resistance under water stress. Journal Agricultural University of Hebei 25, 1–3. [in Chinese]
Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant, Cell & Environment 34, 738–751.
| The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVGks7s%3D&md5=98706a3312eab1a74ab35365e27f30e1CAS |
Lohmann C, Eggers-Schumacher G, Wunderlich M, Schöffl F (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Molecular Genetics and Genomics 271, 11–21.
| Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Kktb4%3D&md5=40fa3cf96ed414d0f43a99a4241eb151CAS | 14655047PubMed |
Meir S, Philosph-Hadas S, Aharoni N (1992) Ethylene-increased accumulation of fluorescent lipid-peroxidation products detected during senescence of parsley by a newly developed method. Journal of the American Society for Horticultural Science 117, 128–132.
Minibaeva FV, Gordon LK (2003) Superoxide production and the activity of extracellular peroxidase in plant tissues under stress conditions. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 411–416.
| Superoxide production and the activity of extracellular peroxidase in plant tissues under stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFyitrc%3D&md5=db7e8951c9e0ee2fbda3fdd60f5f5c1cCAS |
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K (2002) In the complex family of heat stress transcription factors, HSFA1 has a unique role as master regulator of thermotolerance in tomato. Genes & Development 16, 1555–1567.
| In the complex family of heat stress transcription factors, HSFA1 has a unique role as master regulator of thermotolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVGmtb4%3D&md5=fdbca492ed263be3f2e5f32b6c5d297fCAS |
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. The Plant Journal 48, 535–547.
| Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ylurbF&md5=614a45e7b977fe2bbea61a0c62d20a20CAS | 17059409PubMed |
Nishizawa-Yokoi A, Nosaka R, Hayashi H, Tainaka H, Maruta T, Tamoi M, Ikeda M, Ohme-Takagi M, Yoshimura K, Yabuta Y, Shigeoka S (2011) HSFA1d and HSFA1e involved in the transcriptional regulation of HSFA2 function as key regulators for the HSF signaling network in response to environmental stress. Plant & Cell Physiology 52, 933–945.
| HSFA1d and HSFA1e involved in the transcriptional regulation of HSFA2 function as key regulators for the HSF signaling network in response to environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFymsrY%3D&md5=d3ec907b889dc497bdf5bdb435ef4907CAS |
Nover L, Scharf KD, Gagliardi D, Vergne P, Czarnecka-Verne E (1996) The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress & Chaperones 1, 215–223.
| The Hsf world: classification and properties of plant heat stress transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvVOqsQ%3D%3D&md5=b36e315a2059a15eda3cab98bd45f904CAS |
Scharf KD, Rose S, Zott W, Schöffl F, Nover L (1990) Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO Journal 9, 4495–4501.
Scharf KD, Heider H, Höhfeld I, Lyck R, Schmidt E (1998) The tomato HSF system: HSFA2 needs interaction with HSFA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Molecular and Cellular Biology 18, 2240–2251.
Schöffl F, Prändl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiology 117, 1135–1141.
| Regulation of the heat-shock response.Crossref | GoogleScholarGoogle Scholar | 9701569PubMed |
Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D (2006) The heat stress transcription factor HSFA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Molecular Biology 60, 759–772.
| The heat stress transcription factor HSFA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVSgtLo%3D&md5=c066d99f81361d4bec09a4e11131eea5CAS | 16649111PubMed |
Shim D, Hwang JU, Lee J, Lee S, Choi Y (2009) Orthologs of the class A4 heat shock transcription factor HSFA4a confer cadmium tolerance in wheat and rice. The Plant Journal 21, 4031–4043.
Skylas DJ, Cordwell SJ, Hains PG, Larsen MR, Basseal DJ (2002) Heat shock of wheat during grain filling: proteins associated with heat-tolerance. Journal of Cereal Science 35, 175–188.
| Heat shock of wheat during grain filling: proteins associated with heat-tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFOgtb8%3D&md5=e2f971efb3d4114bd6c6db45f8caee31CAS |
Tang ZC (1999) ‘Guide to modern plant physiology experiment.’ (Science Press: Beijing) [in Chinese]
Voellmy R, Boellmann F (2007) Chaperone regulation of the heat shock protein response. Advances in Experimental Medicine and Biology 594, 89–99.
| Chaperone regulation of the heat shock protein response.Crossref | GoogleScholarGoogle Scholar | 17205678PubMed |
Vranova E, Inze D, van Breusegem F (2002) Signal transduction during oxidative stress. Journal of Experimental Botany 53, 1227–1236.
| Signal transduction during oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFSls7w%3D&md5=7eb6cd3250d733cfe49e5277351b7725CAS | 11997371PubMed |
Xue GP, Sadat S, Drenth J, Mcintyre CL (2014) The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. Journal of Experimental Botany 65, 539–557.
| The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Chs7Y%3D&md5=bd604d8cfde6b22c66173838e932e014CAS | 24323502PubMed |
Xue GP, Drench J, McIntyre CL (2015) TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. Journal of Experimental Botany 66, 1025–1039.
| TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets.Crossref | GoogleScholarGoogle Scholar | 25428996PubMed |
Yamanouchi U, Yano M, Lin HX, Ashikari M, Yamada K (2002) Rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proceedings of the National Academy of Sciences of the United States of America 99, 7530–7535.
| Rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlCkurY%3D&md5=18bb831150f23436810c24af925f3d00CAS | 12032317PubMed |
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H (2008) Expression of rice heat stress transcription factor OsHSFA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227, 957–967.
| Expression of rice heat stress transcription factor OsHSFA2e enhances tolerance to environmental stresses in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsF2isLc%3D&md5=a927a3638b1e9e8d2e32da24bdd6e02bCAS | 18064488PubMed |
Zhang SX, Xu ZS, Li PS, Yang L, Wei YQ (2013) Overexpression of TaHSF3 in transgenic Arabidopsis enhances tolerance to extreme temperatures. Plant Molecular Biology Reporter 31, 688–697.
| Overexpression of TaHSF3 in transgenic Arabidopsis enhances tolerance to extreme temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvVKmt70%3D&md5=ce5b0b4acafdbff809cc927d6d3283c7CAS |