Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass

Plant Physiology

Volumn 161, Issue 3, 2013, Pages 1375-1391

  Zhou, Man ^a   Li, Dayong ^b   Li, Zhigang ^a   Hu, Qian ^a   Yang, Chunhua ^b   Zhu, Lihuang ^b   Luo, Hong ^a  

^a CLEMSON UNIVERSITY   (United States)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874639087     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.208702     Document Type: Article

References (98)

1. Asch F, Dingkuhn M, Dörffling K, Miezan K (2000) Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice. Euphytica 113: 109-118
2. Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13: 343-349
3. Bolaños J, Edmeades G (1993) Eight cycles of selection for drought tolerance in lowland tropical maize. II. Responses in reproductive behavior. Field Crops Res 31: 253-268
4. Bondada BR, Oosterhuis DM, Murphy JB, Kim KS (1996) Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract, and boll. Environ Exp Bot 36: 61-69
5. Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. J Exp Bot 53: 13-25
6. +exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143: 1918-1928
7. Campos H, Cooper M, Habben J, Edmeades G, Schussler J (2004) Improving drought tolerance in maize: a view from industry. Field Crops Res 90: 19-34
8. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101: 9909-9914
9. Chandra Babu R, Zhang J, Blum A, David Ho TH, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166: 855-862
10. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot (Lond) 103: 551-560
11. Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57: 1059-1078
12. Deák C, Jäger K, Fábián A, Nagy V, Albert Z, Miskó A, Barnabás B, Papp I (2011) Investigation of physiological responses and leaf morphological traits of wheat genotypes with contrasting drought stress tolerance. Acta Biologica Szegediensis 55: 69-71
13. de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12: 474-481
14. Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot (Lond) 103: 29-38
15. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55: 307-319
16. Fu D, Huang B, Xiao Y, Muthukrishnan S, Liang GH (2007) Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Rep 26: 467-477
17. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99: 15898-15903
18. +-pump. Proc Natl Acad Sci USA 98: 11444-11449
19. Haynes RJ (1980) A comparison of two modified Kjeldahl digestion techniques for multi-element plant analysis with conventional wet and dry ashing methods. Commun Soil Sci Plant Anal 11: 459-467
20. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103: 12987-12992
21. Huang S, Spielmeyer W, Lagudah ES, James RA, Platten JD, Dennis ES, Munns R (2006) A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142: 1718-1727
22. Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23: 1805-1817
23. Javaux M, Schroder T, Vanderborght J, Vereecken H (2008) Use of a threedimensional detailed modeling approach for predicting root water uptake. Vadose Zone J 7: 1079-1088
24. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799
25. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53
26. Khraiwesh B, Zhu J-K, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819: 137-148
27. Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lü S, Joubès J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151: 1918-1929
28. Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22: 3574-3588
29. Läuchli A, (1984) Salt exclusion: an adaptation of legumes for crops and pastures under saline conditions. In RC Staples, GH Toenniessen, eds, Salinity Tolerance in Plants-Strategies for Crop Improvement. Wiley, New York, pp 171-187
30. Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32: 139-149
31. Lewis R, Mendu V, Mcnear D, Tang G (2009) Roles of microRNAs in plant abiotic stress. In SM Jain, DS Brar, eds, Molecular Techniques in Crop Improvement, Ed 2. Springer, Cambridge, pp 357-372
32. +-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant Cell Environ 33: 272-289
33. Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45: 481-489
34. Lindsay MP, Lagudah ES, Hare RA, Munns R (2004) A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol 31: 1105-1114
35. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836-843
36. Lu X-Y, Huang X-L (2008) Plant miRNAs and abiotic stress responses. Biochem Biophys Res Commun 368: 458-462
37. Luo H, Hu Q, Nelson K, Longo C, Kausch A (2004a) Controlling transgene escape in genetically modified grasses. In A Hopkins, Z-Y Wang, R Mian, M Sledge, R Barker, eds, Molecular Breeding of Forage and Turf, Vol 11. Springer, Dordrecht, The Netherlands, pp 245-254
38. Luo H, Hu Q, Nelson K, Longo C, Kausch AP, Chandlee JM, Wipff JK, Fricker CR (2004b) Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Rep 22: 645-652
39. Luo H, Kausch A, Hu Q, Nelson K, Wipff J, Fricker C, Owen T, Moreno M, Lee J, Hodges T (2005) Controlling transgene escape in GM creeping bentgrass. Mol Breed 16: 185-188
40. Lutts S, Kinet J, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot (Lond) 78: 389-398
41. Lv D-K, Bai X, Li Y, Ding X-D, Ge Y, Cai H, Ji W, Wu N, Zhu Y-M (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459: 39-47
42. Manschadi AM, Christopher J, Hammer GL (2006) The role of root architectural traits in adaptation of wheat to water-limited environments. Funct Plant Biol 33: 823-837
43. Manschadi AM, Hammer GL, Christopher JT, DeVoil P (2008) Genotypic variation in seedling root architectural traits and implications for drought adaptation in wheat (Triticum aestivum L.). Plant Soil 303: 115-129
44. Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when posttranscriptional and post-translational regulations control transcription. Plant Sci 174: 420-431
45. +transport in Arabidopsis. Plant Cell 21: 2163-2178
46. Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31: 203-216
47. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25: 239-250
48. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167: 645-663
49. Munns R, Hare RA, James RA, Rebetzke GJ (2000) Genetic variation for improving the salt tolerance of durum wheat. Aust J Agric Res 51: 69-74
50. Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253: 201-218
51. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57: 1025-1043
52. Munns R, Rebetzke GJ, Husain S, James RA, Hare RA (2003) Genetic control of sodium exclusion in durum wheat. Aust J Agric Res 54: 627-635
53. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681
54. Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106: 22534-22539
55. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149: 88-95
56. Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299: 1404-1407
57. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, et al (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104: 16450-16455
58. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138: 341-351
59. Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, et al (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39: 787-791
60. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257-263
61. Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581: 3592-3597
62. Plank CO (1992) Plant analysis reference procedures for the southern region of the United States. Southern Cooperative Series Bulletin No. 368, http://www. ncagr.gov/agronomi/pdffiles/sera368.pdf (December 18, 2008)
63. Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104: 19631-19636
64. Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16: 258-264
65. +selectivity under salt stress. Plant Cell Environ 24: 875-880
66. +nutrition in planta. Plant Physiol 136: 2500-2511
67. Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6: e230
68. Schroder T, JavauxM, Vanderborght J, Korfgen B, Vereecken H (2008) Effect of local soil hydraulic conductivity drop using a three-dimensional root water uptake model. Vadose Zone J 7: 1089-1098
69. +antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21: 81-85
70. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227
71. Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779: 743-748
72. Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12: 301-309
73. Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17: 196-203
74. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019
75. Tardieu F (1996) Drought perception by plants: do cells of droughted plants experience water stress? Plant Growth Regul 20: 93-104
76. Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J Exp Bot 63: 25-31
77. Tardieu F, Bruckler L, Lafolie F (1992) Root clumping may affect the root water potential and the resistance to soil-root water transport. Plant Soil 140: 291-301
78. +transport in higher plants. Ann Bot (Lond) 91: 503-527
79. Thiebaut F, Rojas CA, Almeida KL, Grativol C, Domiciano GC, Lamb CRC, Engler JdeA, Hemerly AS, Ferreira PCG (2012) Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ 35: 502-512
80. Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49: 547-555
81. Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3: 12
82. Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162: 465-472
83. Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12: 367
84. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1-14
85. White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: a review. Ann Bot (Lond) 88: 967-988
86. +antiporter plays an important role in salt stress. Plant Cell Physiol 45: 600-607
87. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21: 3421-3435
88. Xiao H, Wang Y, Liu D, Wang W, Li X, Zhao X, Xu J, Zhai W, Zhu L (2003) Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference. Plant Mol Biol 52: 957-966
89. Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol Plant 3: 469-490
90. Yeo A, Flowers T (1983) Varietal differences in the toxicity of sodium ions in rice leaves. Physiol Plant 59: 189-195
91. Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289: 3-16
92. Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19: 765-768
93. Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salttolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98: 12832-12836
94. 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). Plant J 42: 689-707
95. Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field: using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135: 615-621
96. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354: 585-590
97. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61: 4157-4168
98. Zhou X-J, Zhao H-B, Ma C-C, Li Q-F (2009) Effects of exogenous silicon on leaf structure and water-holding capacity of cucumber plants. Chin J Ecol 28: 556-559