Distinct transcriptional profiles of ozone stress in soybean (Glycine max) flowers and pods

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Leisner, Courtney P ^a   Ming, Ray ^a   Ainsworth, Elizabeth A ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b USDA ARS Global Change and Photosynthesis Research Unit   (United States)

Author keywords

Cell wall modification; Glycine max; Matrix metalloproteinases; Oxidative stress; RNA Sequencing

Indexed keywords

OZONE; TRANSCRIPTOME;

DRUG EFFECTS; FLOWER; FRUIT; METABOLISM; PHYSIOLOGICAL STRESS; SOYBEAN;

FLOWERS; FRUIT; OZONE; SOYBEANS; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84964312801     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0335-y     Document Type: Article

References (89)

1. Van Dingenen R, Dentener FJ, Raes F, Krol MC, Emberson L, Cofala J: The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmos Environ 2009, 43:604-618.
2. Anenberg SC, Horowitz LW, Tong DQ, West JJ: An estimate of the global burden of anthropogenic ozone and fine particulate matter on premature human mortality using atmospheric modeling. Environ Health Persp 2010, 118:1189-1195.
3. The Royal Society: Ground-level ozone in the 21st century: future trends, impacts and policy implications. In Sci Policy Rep 15/08, R. Soc. London; 2008:1-132.
4. Young PJ, Archibald AT, Bowman KW, Lamarque J-F, Naik V, Stevenson DS, Tilmes S, Voulgarakis A, Wild O, Bergmann D, Cameron-Smith P, Cionni I, Collins WJ, Dalsoren SB, Doherty RM, Eyring V, Faluvegi G, Horowitz LW, Josse B, Lee YH, MacKenzie IA, Nagashima T, Plummer DA, Righi M, Rumbold ST, Skeie RB, Shindell DT, Strode SA, Sudo K, Szopa S, et al: Pre-industrial to end 21st century projections of tropospheric ozone from the Atmospheric Chemistry and Climate Model Intercomparison Project (ACCMIP). Atmos Chem Phys 2013, 13:2063-2090.
5. Emberson LD, Buker P, Ashmore MR, Mills G, Jackson LS, Agrawal M, Atikuzzaman MD, Cinderby S, Engardt M, Jamir C, Kobayashi K, Oanh NTK, Quadir QF, Wahid A: A comparison of North American and Asian exposure-response data for ozone effects on crop yields. Atmos Environ 2009, 43:1945-1953.
6. Kangasjarvi J, Jaspers P, Kollist H: Signalling and cell death in ozoneexposed plants. Plant Cell Environ 2005, 28:1021-1036.
7. Ainsworth EA, Yendrek CR, Sitch S, Collins WJ, Emberson LD: The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 2012, 63:637-661.
8. Wilkinson S, Mills G, Illidge R, Davies WJ: How is ozone pollution reducing our food supply? J Exp Bot 2012, 63:527-536.
9. Black VJ, Black CR, Roberts JA, Stewart CA: Impact of ozone on the reproductive development of plants. New Phytol 2000, 147:421-447.
10. Ashmore MR: Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 2005, 28:949-964.
11. Leisner CP, Ainsworth EA: Quantifying the effects of ozone on plant reproductive growth and development. Global Change Biol 2012, 18:606-616.
12. Stewart CA, Black VJ, Black CR, Roberts JA: Direct effects of ozone on the reproductive development of Brassica species. J Plant Physiol 1996, 148:172-178.
13. Liu FL, Andersen MN, Jensen CR: Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Funct Plant Biol 2003, 30:271-280.
14. van Schaik PH, Probst AH: Effects of some environmental factors on flower production and reproductive efficiency in soybeans. Agron J 1958, 50:192-197.
15. Hansen WR, Shibles R: Seasonal log of flowering and podding activity of field-grown soybeans. Agron J 1978, 70:47-50.
16. Wiebold WJ, Ashley DA, Boerma HR: Reproductive abscission levels and patterns for eleven determinate soybean cultivars. Agron J 1981, 73:43-46.
17. Huff A, Dybing CD: Factors affecting shedding of flowers in soybean (Glycine max (L.) Merrill). J Exp Bot 1980, 31:751-762.
18. Heindl JC, Brun WA: Patterns of reproductive abscission, seed yield, and yield components in soybean. Crop Sci 1984, 24:542-545.
19. Brun WA, Betts KJ: Source/sink relations of abscising and nonabscising soybean flowers. Plant Physiol 1984, 75:187-191.
20. Carlson DR, Dyer DJ, Cotterman CD, Durley RC: The physiological basis for cytokinin induced increases in pod set in IX93-100 soybeans. Plant Physiol 1987, 84:233-239.
21. Nagel L, Brewster R, Riedell WE, Reese RN: Cytokinin regulation of flower and pod set in soybeans (Glycine max (L.) Merr.). Ann Bot London 2001, 88:27-31.
22. Jiang HF, Egli DB: Shade induced changes in flower and pod number and flower and fruit abscission in soybean. Agron J 1993, 85:221-225.
23. Westgate ME, Peterson CM: Flower and pod development in waterdeficient soybeans (Glycine max L. Merr.). J Exp Bot 1993, 44:109-117.
24. Kokubun M, Shimada S, Takahashi M: Flower abortion caused by preanthesis water deficit is not attributed to impairment of pollen in soybean. Crop Sci 2001, 41:1517-1521.
25. Cheng Y-Q, Liu J-F, Yang X, Ma R, Liu C, Liu Q: RNA-seq analysis reveals ethylene-mediated reproductive organ development and abscission in soybean (Glycine max L. Merr.). Plant Mol Biol Rep 2013, 31:607-619.
26. Tuomainen J, Betz C, Kangasjarvi J, Ernst D, Yin Z-H, Langebartels C, Sangermann H: Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J 1997, 12:1151-1162.
27. Betzelberger AM, Yendrek CR, Sun J, Leisner CP, Nelson RL, Ort DR, Ainsworth EA: Ozone exposure response for U.S. soybean cultivars: Linear reductions in photosynthetic potential, biomass and yield. Plant Physiol 2012, 160:1827-1839.
28. Sharma YK, Davis KR: Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 1994, 105:1089-1096.
29. Sharma YK, Leon J, Raskin I, Davis KR: Ozone-induced responses in Arabidopsis thaliana: The role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci U S A 1996, 93:5099-5104.
30. Eckey-Kaltenbach H, Kiefer E, Grosskopf E, Ernst D, Sandermann H: Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant Mol Biol 1997, 33:343-350.
31. Miller JD, Arteca RN, Pell EJ: Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 1999, 120:1015-1023.
32. Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV: Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 2003, 4:R20.
33. Tamaoki M, Nakajima N, Kubo A, Aono M, Matsuyama T, Saji H: Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 2003, 53:443-456.
34. Baier M, Kandlbinder A, Golldack D, Dietz KJ: Oxidative stress and ozone: perception, signalling and response. Plant Cell Environ 2005, 28:1012-1020.
35. Gillespie KM, Xu FX, Richter KT, McGrath JM, Markelz RJC, Ort DR, Leakey ADB, Ainsworth EA: Greater antioxidant and respiratory metabolism in field-grown soybean exposed to elevated O3 under both ambient and elevated CO2. Plant Cell Environ 2012, 35:169-184.
36. Andrews AD, Svec LV: Photosynthetic activity of soybean pods at different growth stages compared to leaves. Can J Plant Sci 1975, 55:501-505.
37. Horner HT, Healy RA, Cervantes-Martinez T, Palmer RG: Floral nectary fine structure and development in Glycine max L. (Fabaceae). Int J Plant Sci 2003, 164:675-690.
38. Mann JD, Jaworski EG: Comparison of stresses which may limit soybean yields. Crop Sci 1970, 10:620-624.
39. Sionit N, Kramer PJ: Effect of water stress during different stages of growth of soybean. Agron J 1977, 69:274-278.
40. Shiu SH, Bleecker AB: Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 2001, 98:10763-10768.
41. Shiu SH, Bleecker AB: Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 2003, 132:530-543.
42. Wrzaczek M, Brosche M, Salojarvi J, Kangasjarvi S, Idanheimo N, Mersmann S, Robatzek S, Karpinski S, Karpinska B, Kangasjarvi J: Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 2010, 10:95.
43. Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y, Hu Y: The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biol 2013, 13:148.
44. Llorca CM, Potschin M, Zentgraf U: bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front Plant Sci 2014, 5:169.
45. Olbrich M, Betz G, Gerstner E, Langebartels C, Sandermann H, Ernst D: Transcriptome analysis of ozone-responsive genes in leaves of European beech (Fagus sylvatica L.). Plant Biol 2005, 7:670-676.
46. Rizzo M, Bernardi R, Salvini M, Nali C, Lorenzini G, Durante M: Identification of differentially expressed genes induced by ozone stress in sensitive and tolerant poplar hybrids. J Plant Physiol 2007, 164:945-949.
47. Pandey V, Haikio E, Lehesranta S, Koistinen K, Karenlampi S, Oksanen E: Proteomic analysis of two hybrid aspen clones subjected to long-term chronic ozone exposure in open field. Curr Proteomics 2013, 10:67-74.
48. Pak JH, Liu CY, Huangpu J, Graham JS: Construction and characterization of the soybean leaf metalloproteinase cDNA. FEBS Lett 1997, 404:283-288.
49. Delorme VGR, McCabe PF, Kim DJ, Leaver CJ: A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiol 2000, 123:917-927.
50. Liu YQ, Dammann C, Bhattacharyya MK: The matrix metalloproteinase gene GmMMP2 is activated in response to pathogenic infections in soybean. Plant Physiol 2001, 127:1788-1797.
51. Combier JP, Vernie T, de Billy F, El Yahyaoui F, Mathis R, Gamas P: The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiol 2007, 144:703-716.
52. Jiang WP, Bond JS: Families of metalloendopeptidases and their relationships. FEBS Lett 1992, 312:110-114.
53. Bode W, Gomisruth FX, Stockler W: Astacins, serralysins, snake-venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-Turn) and topologies and should be grouped into a common family, the metzincins. FEBS Lett 1993, 331:134-140.
54. Hooper NM: Families of zinc metalloproteases. FEBS Lett 1994, 354:1-6.
55. Graham JS, Xiong J, Gillikin JW: Purification and developmental analysis of a metalloendoproteinase from the leaves of Glycine max. Plant Physiol 1991, 97:786-792.
56. McGeehan G, Burkhart W, Anderegg R, Becherer JD, Gillikin JW, Graham JS: Sequencing and characterization of the soybean leaf metalloproteinase-structural and functional similarity to the matrix metalloproteinase family. Plant Physiol 1992, 99:1179-1183.
57. Rowsell S, Hawtin P, Minshull CA, Jepson H, Brockbank SMV, Barratt DG, Slater AM, McPheat WL, Waterson D, Henney AM, Pauptit RA: Crystal structure of human MMP9 in complex with a reverse hydroxamate inhibitor. J Mol Biol 2002, 319:173-181.
58. Ranieri A, Castagna A, Pacini J, Baldan B, Mensuali-Sodi A, Soldatini GF: Early production and scavenging of hydrogen peroxide in the apoplast of sunflower plants exposed to ozone. J Exp Bot 2003, 54:2529-2540.
59. Flinn BS: Plant extracellular matrix metalloproteinases. Funct Plant Biol 2008, 35:1183-1193.
60. Afzal AJ, Wood AJ, Lightfoot DA: Plant receptor-like serine threonine kinases: Roles in signaling and plant defense. Mol Plant Microbe 2008, 21:507-517.
61. ten Hove CA, Bochdanovits Z, Jansweijer VMA, Koning FG, Berke L, Sanchez-Perez GF, Scheres B, Heidstra R: Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T-DNA insertion set. Plant Mol Biol 2011, 76:69-83.
62. Greeff C, Roux M, Mundy J, Petersen M: Receptor-like kinase complexes in plant innate immunity. Front Plant Sci 2012, 3:A209.
63. Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K: Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 2012, 70:599-613.
64. Zhang XJ, Yang GY, Shi R, Han XM, Qi LW, Wang RG, Xiong LM, Li GJ: Arabidopsis cysteine-rich receptor-like kinase 45 functions in the responses to abscisic acid and abiotic stresses. Plant Physiol Bioch 2013, 67:189-198.
65. Yang L, Wu KC, Gao P, Liu XJ, Li GP, Wu ZJ: GsLRPK, a novel cold-activated leucine-rich repeat receptor-like protein kinase from Glycine soja, is a positive regulator to cold stress tolerance. Plant Sci 2014, 215:19-28.
66. Babosha AV: Inducible lectins and plant resistance to pathogens and abiotic stress. Biochem Mosc 2008, 73:812-825.
67. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP: Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 2013, 64:445-458.
68. Nishitani K: Implication of xyloglucan related protein (XRP) family in regulation of plant growth and development. Trends Glycosci Glycotech 1997, 9:233-234.
69. Matsui A, Yokoyama R, Seki M, Ito T, Shinozaki K, Takahashi T, Komeda Y, Nishitani K: AtXTH27 plays an essential role in cell wall modification during the development of tracheary elements. Plant J 2005, 42:525-534.
70. Jimenez T, Martin I, Labrador E, Dopico B: The immunolocation of xyloglucan endotransglucosylase/hydrolase specific to elongating tissues in Cicer arietinum suggests a role in the elongation of vascular cells. J Exp Bot 2006, 57:3979-3988.
71. Romo S, Jimenez T, Labrador E, Dopico B: The gene for a xyloglucan endotransglucosylase/hydrolase from Cicer arietinum is strongly expressed in elongating tissues. Plant Physiol Biochem 2005, 43:169-176.
72. Hyodo H, Yamakawa S, Takeda Y, Tsuduki M, Yokota A, Nishitani K, Kohchi T: Active gene expression of a xyloglucan endotransglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol Biol 2003, 52:473-482.
73. Liu YB, Lu SM, Zhang JF, Liu S, Lu YT: A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 2007, 226:1547-1560.
74. Malinowski R, Filipecki M, Tagashira N, Wisniewska A, Gaj P, Plader W, Malepszy S: Xyloglucan endotransglucosylase/hydrolase genes in cucumber (Cucumis sativus)-differential expression during somatic embryogenesis. Physiol Plant 2004, 120:678-685.
75. Singh AP, Tripathi SK, Nath P, Sane AP: Petal abscission in rose is associated with the differential expression of two ethylene-responsive xyloglucan endotransglucosylase/hydrolase genes, RbXTH1 and RbXTH2. J Exp Bot 2011, 62:5091-5103.
76. Kumpf RP, Shi CL, Larrieu A, Sto IM, Butenko MA, Peret B, Riiser ES, Bennett MJ, Aalen RB: Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proc Natl Acad Sci U S A 2013, 110:5235-5240.
77. Jinn TL, Stone JM, Walker JC: HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Gene Dev 2000, 14:108-117.
78. Olbrich M, Gerstner E, Welzl G, Winkler JB, Ernst D: Transcript responses in leaves of ozone-treated beech saplings seasons at an outdoor free air model fumigation site over two growing seasons. Plant Soil 2009, 323:61-74.
79. Wu YJ, Jeong BR, Fry SC, Boyer JS: Change in XET activities, cell wall extensibility and hypocotyl elongation of soybean seedlings at low water potential. Planta 2005, 220:593-601.
80. Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B: Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ 2008, 31:1592-1605.
81. Hewitt EJ: Sand and water culture methods used in the study of plant nutrition. London: Commonwealth Agricultural Bureau; 1952.
82. Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
83. Bullard JH, Purdom E, Hansen KD, Dudoit S: Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics 2010, 11:94.
84. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, Keime C, Marot G, Castel D, Estelle J, Guernec G, Jagla B, Jouneau L, Laloë D, Le Gall C, Schaëffer B, Le Crom S, Guedj M, Jaffrézic F: A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief Bioinform 2013, 14:671-683.
85. Shapiro SS, Wilk MB: An analysis of variance test for normality (complete samples). Biometrika 1965, 52:591-611.
86. Benjamini Y, Hochberg Y: Controlling the false discovery rate-a practical and powerful approach to multiple testing. J Royal Stat Soc Series B Method 1995, 57:289-300.
87. Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
88. Simossis VA, Heringa J: PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res 2005, 33:289-294.
89. Combet C, Blanchet C, Geourjon C, Deleage G: NPS: Network protein sequence analysis. Trends Biochem Sci 2000, 25:147-150.