#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Physiological and molecular responses to drought stress in teak (Tectona grandis L.f.)


Autoři: Esteban Galeano aff001;  Tarcísio Sales Vasconcelos aff001;  Perla Novais de Oliveira aff001;  Helaine Carrer aff001
Působiště autorů: Department of Biological Sciences, Luiz de Queiroz College of Agriculture (ESALQ), University of Sao Paulo, Piracicaba, Brazil aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221571

Souhrn

Drought stress is an increasingly common and worrying phenomenon because it causes a loss of production in both agriculture and forestry. Teak is a tropical tree which needs alternating rainy and dry seasons to produce high-quality wood. However, a robust understanding about the physiological characteristics and genes related to drought stress in this species is lacking. Consequently, after applying moderate and severe drought stress to teak seedlings, an infrared gas analyzer (IRGA) was used to measure different parameters in the leaves. Additionally, using the root transcriptome allowed finding and analyzing the expression of several drought-related genes. As a result, in both water deficit treatments a reduction in photosynthesis, transpiration, stomatal conductance and leaf relative water content was found. As well, an increase in free proline levels and intrinsic water use efficiency was found when compared to the control treatment. Furthermore, 977 transcripts from the root contigs showed functional annotation related to drought stress, and of these, TgTPS1, TgDREB1, TgAREB1 and TgPIP1 were selected. The expression analysis of those genes along with TgHSP1, TgHSP2, TgHSP3 and TgBI (other stress-related genes) showed that with moderate treatment, TgTPS1, TgDREB1, TgAREB1, TgPIP1, TgHSP3 and TgBI genes had higher expression than the control treatment, but with severe treatment only TgTPS1 and TgDREB1 showed higher expression than the control treatment. At the end, a schematic model for the physiological and molecular strategies under drought stress in teak from this study is provided. In conclusion, these physiological and biochemical adjustments in leaves and genetic changes in roots under severe and prolonged water shortage situations can be a limiting factor for teak plantlets’ growth. Further studies of those genes under different biotic and abiotic stress treatments are needed.

Klíčová slova:

Biology and life sciences – Cell biology – Genetics – Gene expression – Biochemistry – Plant science – Plant pathology – Cellular structures and organelles – Cell membranes – Membrane proteins – Ecology and environmental sciences – Plant ecology – Plant-environment interactions – Ecology – Plant physiology – Plant defenses – Plant resistance to abiotic stress – Plant anatomy – Leaves – Stomata – Stem anatomy – Plant biochemistry – Photosynthesis – Natural resources – Water resources


Zdroje

1. Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol. 2003;30: 239–264. doi: 10.1071/FP02076

2. Breshears DD, McDowell NG, Goddard KL, Dayem KE, Martens SN, Meyer CW, et al. Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology. 2008;89: 41–47. doi: 10.1890/07-0437.1 18376545

3. Belhassen E. Drought tolerance in higher plants: genetical, physiological and molecular biological analysis. 1st ed. Belhassen E, editor. Dordrecht: Springer; 1997. doi: 10.1007/978-94-017-1299-6

4. Seki M, Umezawa T, Urano K, Shinozaki K. Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol. 2007;10: 296–302. doi: 10.1016/j.pbi.2007.04.014 17468040

5. Xu Z, Zhou G, Shimizu H. Are plant growth and photosynthesis limited by pre-drought following rewatering in grass? J Exp Bot. 2009;60: 3737–3749. doi: 10.1093/jxb/erp216 19596698

6. Krasensky J, Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot. 2012;63: 1593–1608. doi: 10.1093/jxb/err460 22291134

7. Agarwal PK, Agarwal P, Reddy MK, Sopory SK. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 2006;25: 1263–1274. doi: 10.1007/s00299-006-0204-8 16858552

8. Delorge I, Janiak M, Carpentier S, Van Dijck P. Fine tuning of trehalose biosynthesis and hydrolysis as novel tools for the generation of abiotic stress tolerant plants. Front Plant Sci. 2014;5: 1–9. doi: 10.3389/fpls.2014.00147 24782885

9. Maurel C, Verdoucq L, Luu D-T, Santoni V. Plant Aquaporins: Membrane Channels with Multiple Integrated Functions. Annu Rev Plant Biol. 2008;59: 595–624. doi: 10.1146/annurev.arplant.59.032607.092734 18444909

10. Ishikawa T, Watanabe N, Nagano M, Kawai-Yamada M, Lam E. Bax inhibitor-1: A highly conserved endoplasmic reticulum-resident cell death suppressor. Cell Death Differ. Nature Publishing Group; 2011;18: 1271–1278. doi: 10.1038/cdd.2011.59 21597463

11. Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen T, et al. An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol. 2010;186: 681–695. doi: 10.1111/j.1469-8137.2010.03207.x 20298483

12. Lu P-P, Yu T-F, Zheng W-J, Chen M, Zhou Y-B, Chen J, et al. The Wheat Bax Inhibitor-1 Protein Interacts with an Aquaporin TaPIP1 and Enhances Disease Resistance in Arabidopsis. Front Plant Sci. 2018;9: 1–16. doi: 10.3389/fpls.2018.00020 29403525

13. Tanaka K, Tanaka N, Matsuo N, Tantasirin C, Masakazu S. Impacts of irrigation on the deciduous period of teak (Tectona grandis) in a monsoonal climate. Can J For Res. 2017;47: 1193–1201. doi: 10.1139/cjfr-2017-0122

14. Rajendrudu G, Naidu C V. Leaf gas exchange capacity in relation to leaf position on the stem in field grown teak (Tectona grandis L.f.). Photosynthetica. 1997. pp. 45–55. doi: 10.1023/A:1006859700565

15. Alcântara BK, Veasey EA. Genetic diversity of teak (Tectona grandis L. f.) from different provenances using microsatellite markers. Rev Árvore. 2013;37: 747–758.

16. Fofana IJ, Ofori D, Poitel M, Verhaegen D. Diversity and genetic structure of teak (Tectona grandis L.f) in its natural range using DNA microsatellite markers. New For. 2009;37: 175–195. doi: 10.1007/s11056-008-9116-5

17. Fofana IJ, Lidah YJ, Diarrassouba N, Nguetta SP a, Sangare A, Verhaegen D. Genetic structure and conservation of Teak (Tectona grandis) plantations in Côte d’Ivoire, revealed by site specific recombinase (SSR). Trop Conserv Sci. 2008;1: 279–292.

18. Minn Y, Prinz K, Finkeldey R. Genetic variation of teak (Tectona grandis Linn. f.) in Myanmar revealed by microsatellites. Tree Genet Genomes. 2014;10: 1435–1449. doi: 10.1007/s11295-014-0772-7

19. Tambarussi EV, Rogalski M, Galeano E, Brondani GE, de Martin VDF, da Silva LA, et al. Efficient and new method for tectona grandis in vitro regeneration. Crop Breed Appl Biotechnol. 2017;17. doi: 10.1590/1984-70332017v17n2a19

20. Tiwari SK, Tiwari KP, Siril E a. An improved micropropagation protocol for teak. Plant Cell Tissue Organ Cult. 2002;71: 1–6. doi: 10.1023/A:1016570000846

21. Gangopadhyay G, Gangopadhyay SB, Poddar R, Gupta S, Mukherjee KK. Micropropagation TEAK genetic fidelity.pdf. Biol Plant. 2003;46: 459–461.

22. Hansen OK, Changtragoon S, Ponoy B, Kjær ED, Minn Y, Finkeldey R, et al. Genetic resources of teak (Tectona grandis Linn. f.)—strong genetic structure among natural populations. Tree Genet Genomes. 2015;11: 802. doi: 10.1007/s11295-014-0802-5

23. Galeano E, Vasconcelos TS, Ramiro DA, De Martin VDF, Carrer H. Identification and validation of quantitative real-time reverse transcription PCR reference genes for gene expression analysis in teak (Tectona grandis L.f.). BMC Res Notes. 2014;7: 464. doi: 10.1186/1756-0500-7-464 25048176

24. Diningrat DS, Widiyanto SM, Pancoro A,. I, Shim D, Panchangam B, et al. Identification of Terminal Flowering1 (TFL1) Genes Associated with the Teak (Tectona grandis) Floral Development Regulation Using RNA-seq. Res J Bot. Science Alert; 2015;10: 1–13. doi: 10.3923/rjb.2015.1.13

25. Galeano E, Vasconcelos TS, Carrer H. Characterization of Cinnamyl Alcohol Dehydrogenase gene family in lignifying tissues of Tectona grandis L.f. Silvae Genet. 2018;67: 1–11. doi: 10.2478/sg-2018-0001

26. Camel V, Galeano E, Carrer H. In silico Analysis and Gene Expression of TgNAC01 Transcription Factor Involved in Xylogenesis and Abiotic Stress in Tectona grandis. Acta Biológica Colomb. 2017;22: 359–369.

27. Diningrat DS, Widiyanto SM, Pancoro A,. I, Shim D, Panchangam B, et al. Transcriptome of Teak (Tectona grandis, L.f) in Vegetative to Generative Stages Development. J Plant Sci. 2015;10: 1–14. doi: 10.3923/jps.2015.1.14

28. Yasodha R, Vasudeva R, Balakrishnan S, Sakthi AR, Abel N, Binai N, et al. Draft genome of a high value tropical timber tree, Teak (Tectona grandis L. f): insights into SSR diversity, phylogeny and conservation. DNA Res. 2018;0: 1–11. doi: 10.1093/dnares/dsy013 29800113

29. Zhao D, Hamilton JP, Bhat WW, Johnson SR, Godden GT, Kinser TJ, et al. A chromosomal-scale genome assembly of Tectona grandis reveals the importance of tandem gene duplication and enables discovery of genes in natural product biosynthetic pathways. Gigascience. 2019;8: 1–10. doi: 10.1093/gigascience/giz005 30698701

30. Sneha C, Santhoshkumar A V, Sunil KM. Effect of controlled irrigation on physiological and biometric characteristics in teak (Tectona grandis) seedlings. J Stress Physiol Biochem. 2012;8: 196–202.

31. Okunomo K. Effect of watering regimes and levels of urea fertilizer application on establishment of teak seedlings in an acidic soil. Niger J Res Prod. 2010;16: 1–12.

32. Rajendrudu G, Naidu C V. Effects of water stress on leaf growth and photosynthetic and transpiration rates of Tectona grandis [Internet]. Biologia Plantarum. 1997. pp. 229–234. Available: http://www.springerlink.com/index/Q45741M879753846.pdf

33. Husen A. Growth characteristics, physiological and metabolic responses of teak (Tectona Grandis Linn, f.) clones differing in rejuvenation capacity subjected to drought stress. Silvae Genet. 2010;59: 124–136. doi: 10.1515/sg-2010-0015

34. Ridwan, Handayani T, Riastiwi I, Witjaksono D. Tetraploid Teak Seedling was More Tolerant to Drought Stress than Its Diploid Seedling. J Penelit Kehutan Wallacea. 2018;7: 1–11.

35. Galeano E, Vasconcelos TS, Vidal M, Mejia-Guerra MK, Carrer H. Large-scale transcriptional profiling of lignified tissues in Tectona grandis. BMC Plant Biol. 2015;15. doi: 10.1186/s12870-014-0394-0

36. Turner NC. Crop water deficits: A decade of progress. Adv Agron. 1986;39: 1–51. doi: 10.1016/S0065-2113(08)60464-2

37. Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39: 205–207. doi: 10.1007/BF00018060

38. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8: 1494–512. doi: 10.1038/nprot.2013.084 23845962

39. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson D a, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29: 644–52. doi: 10.1038/nbt.1883 21572440

40. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21: 3674–6. doi: 10.1093/bioinformatics/bti610 16081474

41. Prado CHB a., Moraes J a. PV De. Photosynthetic capacity and specific leaf mass in twenty woody species of Cerrado vegetation under field conditions [Internet]. Photosynthetica. 1997. pp. 103–112. doi: 10.1023/A:1022183423630

42. Turkan I. Plant Responses To Drought and Salinity Stress. 2011.

43. Aroca R. Plant Responses to Drought Stress. From Morphological to Molecular Features. 1st ed. Aroca R, editor. Berlin: Springer; 2012. doi: 10.1007/978-3-642-32653-0

44. Hossain MA, Wani SH, Bhattacharjee S, Burrit DJ, Tran L-SP. Drought Stress Tolerance in Plants, Vol 2. Molecular and Genetic Perspectives [Internet]. 1st ed. Switzerland: Springer; 2016. doi: 10.1007/978-3-319-32423-4

45. Habermann G, Machado EC, Rodrigues JD, Medina CL. CO2 assimilation, photosynthetic light response curves, and water relations of “Pêra” sweet orange plants infected with Xylella fastidiosa. Brazilian J Plant Physiol. 2003;15: 79–87. doi: 10.1590/S1677-04202003000200003

46. Björkman O, Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta. 1987;170: 489–504. doi: 10.1007/BF00402983 24233012

47. Panek JA, Goldstein AH. Response of stomatal conductance to drought in ponderosa pine: implications for carbon and ozone uptake. Tree Physiol. 2001;21: 337–344. doi: 10.1093/treephys/21.5.337 11262925

48. Oliveira AKM, Gualtieri SCJ de, Bocchese RA. Gas exchange of potted Tabebuia aurea plants under hydric stress. Acta Sci Agron. 2011;33: 641–647. doi: 10.4025/actasciagron.v33i4.11254

49. Lawlor DW, Tezara W. Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: A critical evaluation of mechanisms and integration of processes. Ann Bot. 2009;103: 561–579. doi: 10.1093/aob/mcn244 19155221

50. Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, et al. Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol. 2006;172: 73–82. doi: 10.1111/j.1469-8137.2006.01794.x 16945090

51. Chaves MM, Oliveira MM. Mechanisms underlying plant resilience to water deficits: Prospects for water-saving agriculture. J Exp Bot. 2004;55: 2365–2384. doi: 10.1093/jxb/erh269 15475377

52. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol. 2004;6: 269–279. doi: 10.1055/s-2004-820867 15143435

53. Flexas J, Medrano H. Drought-inhibition of photosynthesis in C3plants: Stomatal and non-stomatal limitations revisited. Ann Bot. 2002;89: 183–189. doi: 10.1093/aob/mcf027 12099349

54. Gomes MDMDA Lagôa AMMA, Medina CL Machado EC, Machado MA. Interactions between leaf water potential, stomatal conductance and abscisic acid content of orange trees submitted to drought stress. Brazilian J Plant Physiol. 2004;16: 155–161. doi: 10.1590/S1677-04202004000300005

55. Lima WDP, Jarvis P, Rhizopoulou S. Stomatal Responses of Eucalyptus Species To Elevated Co 2 Concentration and Drought Stress. Sci Agric. 2003;60: 231–238.

56. Santiago LS, Wright SJ. Leaf functional traits of tropical forest plants in relation to growth form. Funct Ecol. 2007;21: 19–27. doi: 10.1111/j.1365-2435.2006.01218.x

57. Zhang J, Nguyen HT, Blum A. Genetic analysis of osmotic adjustment. J Exp Bot. 1999;50: 291–302. doi: 10.1093/jexbot/50.332.291

58. Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot. 2007;59: 206–216. doi: 10.1016/j.envexpbot.2005.12.006

59. DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME. Drought tolerance of two field-grown clones of Coffea canephora. Plant Sci. 2003;164: 111–117. doi: 10.1016/S0168-9452(02)00342-4

60. Lemcoff JH. Osmotic adjustment and its use as a selection criterion in Eucalyptus seedlings. Can J For Res. 1994;24: 2404–2408.

61. Anjum SA, Xie X, Wang L, Saleem MF, Man C, Lei W. Morphological, physiological and biochemical responses of plants to drought stress. African J Agric Res. 2011;6: 2026–2032. doi: 10.5897/AJAR10.027

62. Wang L feng. Physiological and molecular responses to drought stress in rubber tree (Hevea brasiliensis Muell. Arg.). Plant Physiol Biochem. Elsevier Masson SAS; 2014;83: 243–249. doi: 10.1016/j.plaphy.2014.08.012 25194774

63. Guo XY, Zhang XS, Huang ZY. Drought tolerance in three hybrid poplar clones submitted to different watering regimes. J Plant Ecol. 2010;3: 79–87. doi: 10.1093/jpe/rtq007

64. Çamoğlu G. The effects of water stress on evapotranspiration and leaf temperatures of two olive (Olea europaea L.) cultivars. Zemdirbyste-Agriculture. 2013;100: 91–98. doi: 10.13080/z-a.2013.100.012

65. Lawlor DW, Cornic G. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ. 2002;25: 275–294. doi: 10.1046/j.0016-8025.2001.00814.x 11841670

66. Zu X, Lu Y, Wang Q, Chu P, Miao W, Wang H, et al. A new method for evaluating the drought tolerance of upland rice cultivars. Crop J. Elsevier B.V.; 2017;5: 488–498. doi: 10.1016/j.cj.2017.05.002

67. Castro D da S, dos Santos AO, Lobato AK da S, Gouvea DDS, Neto CF de O, da Cunha RLM, et al. Concentrações de Prolina e Carboidratos Solúveis Totais em Folhas Teca (Tectona grandis L.f) Submetida ao Estresse Hídrico. Rev Bras Biociências. 2007;5: 921–923.

68. Moshelion M, Halperin O, Wallach R, Oren R, Way DA. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: Crop water-use efficiency, growth and yield. Plant, Cell Environ. 2015;38: 1785–1793. doi: 10.1111/pce.12410 25039365

69. Nguyen MX, Moon S, Jung KH. Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta. 2013;238: 669–681. doi: 10.1007/s00425-013-1918-9 23801298

70. Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, et al. The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol. 2004;45: 481–489. doi: 10.1093/pcp/pch058 15111723

71. Rodrigues MI, Bravo JP, Sassaki FT, Severino FE, Maia IG. The tonoplast intrinsic aquaporin (TIP) subfamily of Eucalyptus grandis: Characterization of EgTIP2, a root-specific and osmotic stress-responsive gene. Plant Sci. Elsevier Ireland Ltd; 2013;213: 106–113. doi: 10.1016/j.plantsci.2013.09.005 24157213

72. Li J, Ban L, Wen H, Wang Z, Dzyubenko N, Chapurin V, et al. An aquaporin protein is associated with drought stress tolerance. Biochem Biophys Res Commun. Elsevier Ltd; 2015;459: 208–213. doi: 10.1016/j.bbrc.2015.02.052 25701792

73. Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R. PIP1 Plasma Membrane Aquaporins in Tobacco: From Cellular Effects to Function in Plants. Plant Cell. 2002;14: 869–876. doi: 10.1105/tpc.000901 11971141

74. Xu Y, Hu W, Liu J, Zhang J, Jia C, Miao H, et al. A banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses. BMC Plant Biol. 2014;14: 1–14. doi: 10.1186/1471-2229-14-1

75. Liu F, Vantoai T, Moy LP, Bock G, Linford LD, Quackenbush J, et al. Global Transcription Profiling Reveals Comprehensive Insights into Hypoxic Response in Arabidopsis. Plant Physiol. 2005;137: 1115–1129. doi: 10.1104/pp.104.055475 15734912

76. Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC. Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res. 2006;16: 599–608. doi: 10.1038/sj.cr.7310077 16775631

77. Avonce N, Leyman B, Mascorro-Gallardo J, Dijck P V., Thevelein JM, Iturriaga G. The Arabidopsis Trehalose-6-P Synthase AtTPS1 Gene Is a Regulator of Glucose, Abscisic Acid, and Stress Signaling. Plant Physiol. 2004;136: 3649–3659. doi: 10.1104/pp.104.052084 15516499

78. Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant, Cell Environ. 2014;37: 1059–1073. doi: 10.1111/pce.12199 24028172

79. Luo Y, Gao YM, Wang W, Zou CJ. Application of trehalose ameliorates heat stress and promotes recovery of winter wheat seedlings. Biol Plant. 2014;58: 395–398. doi: 10.1007/s10535-014-0397-6

80. Martins LL, Mourato MP, Baptista S, Reis R, Carvalheiro F, Almeida AM, et al. Response to oxidative stress induced by cadmium and copper in tobacco plants (Nicotiana tabacum) engineered with the trehalose-6-phosphate synthase gene (AtTPS1). Acta Physiol Plant. 2014;36: 755–765. doi: 10.1007/s11738-013-1453-0

81. Schluepmann H. Trehalose Mediated Growth Inhibition of Arabidopsis Seedlings Is Due to Trehalose-6-Phosphate Accumulation. Plant Physiol. 2004;135: 879–890. doi: 10.1104/pp.104.039503 15181209

82. Bae MS, Cho EJ, Choi EY, Park OK. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 2003;36: 652–663. doi: 10.1046/j.1365-313X.2003.01907.x 14617066

83. Iordachescu M, Imai R. Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol. 2008;50: 1223–1229. doi: 10.1111/j.1744-7909.2008.00736.x 19017109

84. Zhao D, Hamilton JP, Bhat WW, Johnson SR, Godden GT, Kinser TJ, et al. A chromosomal-scale genome assembly of Tectona grandis reveals the importance of tandem gene duplication and enables discovery of genes in natural product biosynthetic pathways. Gigascience. 2019;giz005: 1–27.

85. Vierling E. The Roles of Heat Shock Proteins in Plants. Annu Rev Plant Biol. 1991;42: 579–620.

86. Wahid A, Gelani S, Ashraf M, Foolad MR. Heat tolerance in plants: An overview. Environ Exp Bot. 2007;61: 199–223. doi: 10.1016/j.envexpbot.2007.05.011

87. Liang M, Chen D, Lin M, Zheng Q, Huang Z, Lin Z, et al. Isolation and characterization of two DREB1 genes encoding dehydration-responsive element binding proteins in chicory (Cichorium intybus). Plant Growth Regul. 2013;73: 45–55. doi: 10.1007/s10725-013-9866-8

88. Rolla AA de P, Carvalho J de FC, Fuganti-Pagliarini R, Engels C, do Rio A, Marin SRR, et al. Phenotyping soybean plants transformed with rd29A:AtDREB1A for drought tolerance in the greenhouse and field. Transgenic Res. 2014;23: 75–87. doi: 10.1007/s11248-013-9723-6 23807320

89. Chen J, Xia X, Yin W. Expression profiling and functional characterization of a DREB2-type gene from Populus euphratica. Biochem Biophys Res Commun. Elsevier Inc.; 2009;378: 483–487. doi: 10.1016/j.bbrc.2008.11.071 19032934

90. Chu Y, Huang Q, Zhang B, Ding C, Su X. Expression and molecular evolution of two DREB1 genes in black poplar (Populus nigra). PLoS One. 2014;9. doi: 10.1371/journal.pone.0098334 24887081

91. Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, et al. Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol. Elsevier; 2009;166: 1544–1556. doi: 10.1016/j.jplph.2009.03.014 19464753

92. Wang X, Chen X, Liu Y, Gao H, Wang Z, Sun G. CkDREB gene in Caragana korshinskii is involved in the regulation of stress response to multiple abiotic stresses as an AP2/EREBP transcription factor. Mol Biol Rep. 2011;38: 2801–2811. doi: 10.1007/s11033-010-0425-3 21127996

93. Navarro M, Ayax C, Martinez Y, Laur J, El Kayal W, Marque C, et al. Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol J. 2011;9: 50–63. doi: 10.1111/j.1467-7652.2010.00530.x 20492548

94. Azzeme AM, Abdullah SNA, Aziz MA, Wahab PEM. Oil palm drought inducible DREB1 induced expression of DRE/CRT- and non-DRE/CRT-containing genes in lowland transgenic tomato under cold and PEG treatments. Plant Physiol Biochem. Elsevier Ltd; 2017;112: 129–151. doi: 10.1016/j.plaphy.2016.12.025 28068641

95. Artlip TS, Wisniewski ME, Bassett CL, Norelli JL. CBF gene expression in peach leaf and bark tissues is gated by a circadian clock. Tree Physiol. 2013;33: 866–877. doi: 10.1093/treephys/tpt056 23956128

96. Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D. Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta. 2011;233: 971–983. doi: 10.1007/s00425-011-1358-3 21274560

97. Ji L, Wang J, Ye M, Li Y, Guo B, Chen Z, et al. Identification and Characterization of the Populus AREB/ABF Subfamily. J Integr Plant Biol. 2013;55: 177–186. doi: 10.1111/j.1744-7909.2012.01183.x 23116154

98. Abdeen A, Schnell J, Miki B. Transcriptome analysis reveals absence of unintended effects in drought-tolerant transgenic plants overexpressing the transcription factor ABF3. BMC Genomics. 2010;11. doi: 10.1186/1471-2164-11-11

99. Hong L, Hu B, Liu X, He CY, Yao Y, Li XL, et al. Molecular cloning and expression analysis of a new stress-related AREB gene from Arachis hypogaea. Biol Plant. 2013;57: 56–62. doi: 10.1007/s10535-012-0236-6

100. Orellana S, Yañez M, Espinoza A, Verdugo I, Gonzalez E, Ruiz-Lara S, et al. The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant, Cell Environ. 2010;33: 2191–2208. doi: 10.1111/j.1365-3040.2010.02220.x 20807374

101. Feng Y, Liang C, Li B, Wan T, Liu T, Cai Y. Differential expression profiles and pathways of genes in drought resistant tree species Prunus mahaleb roots and leaves in response to drought stress. Sci Hortic (Amsterdam). Elsevier; 2017;226: 75–84. doi: 10.1016/j.scienta.2017.07.057

102. Harfouche A, Meilan R, Altman A. Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement. Tree Physiol. 2014;34: 1181–1198. doi: 10.1093/treephys/tpu012 24695726

103. Osakabe Y, Osakabe K, Shinozaki K, Tran L-SP. Response of plants to water stress. Front Plant Sci. 2014;5: 1–8. doi: 10.3389/fpls.2014.00086 24659993

104. Wani SH, Dutta T, Neelapu NRR, Surekha C. Transgenic approaches to enhance salt and drought tolerance in plants. Plant Gene. Elsevier B.V; 2017;11: 219–231. doi: 10.1016/j.plgene.2017.05.006

105. Singh KP, Kushwaha CP. Deciduousness in tropical trees and its potential as indicator of climate change: A review. Ecol Indic. Elsevier Ltd; 2016;69: 699–706. doi: 10.1016/j.ecolind.2016.04.011

106. Ping M, Tuan-hui B, Feng-wang M. Effects of progressive drought on photosynthesis and partitioning of absorbed light in apple trees. J Integr Agric. Chinese Academy of Agricultural Sciences; 2015;14: 681–690. doi: 10.1016/S2095-3119(14)60871-6


Článok vyšiel v časopise

PLOS One


2019 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#