biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 63:733-749, 2019 | DOI: 10.32615/bp.2019.062

Proteome analysis of sesame leaves in response to waterlogging stress at vegetative and flowering stages

H.-J. JUNG1, S.K. ROY1, S.-W. CHO2, S.-J. KWON1, C. KUN3,*, H.-C. CHUN4, S.-H. WOO1,*
1 Department of Crop Science, Chungbuk National University, Cheong-ju, 28644 Republic of Korea
2 Department of Crop Science and Biotechnology, Chonbuk National University, Jeon-ju, 54896 Republic of Korea
3 Center for Research Equipment, Korea Basic Science Institute, Ochang, Cheong-ju, 28119 Republic of Korea
4 National Institute of Crop Science, Rural Development Administration, Miryang, 50424 Republic of Korea

Waterlogging, a major environmental stress, impairs plant growth and development and induces synthesis of different proteins. To understand the molecular mechanisms coupled with morpho-physiological alterations underlying waterlogging tolerance, the LTQ-FTICR MS/MS technique was employed to map the proteomes of leaves of sesame grown under control and waterlogged conditions. The waterlogging treatment caused dramatic alterations in morphological and biochemical properties of the leaves of sesame. For proteome analysis, more than 75 reproducible protein spots were identified on 2-DE gels wherein 51 protein spots (≥ 1.5-fold change) were used for analysis by mass spectrometry. Among 51 differentially abundant proteins, 20 were specific to the 10-leaf stage and 31 were specific to the flowering stage. Most of the differentially abundant proteins were involved in group metabolism, and energy and stress defense. Oxygen-evolving enhancer protein 1, ATP synthase subunit, heat shock proteins, glutamine synthetase, glyceraldehyde-3-phosphate dehydrogenase, and superoxide dismutase were upregulated under waterlogging. However, the photosynthesis- and protein biosynthesis-related proteins (e.g., ribulose-1,5-bisphosphate carboxylase/oxygenase activase, and S-adenosylmethionine synthase 1) were down-regulated under waterlogging. The protein interaction network indicates that energy metabolism- and stress- and defense-related proteins were involved in the protein-protein interaction network, which could form an indispensable network in sesame leaves. To this end, physiological results highlighted the impairment of photosyntheis, which is consistent with results obtained at the proteome level. The upregulation of metabolism-, energy-, and stress defense-related proteins in response to waterlogging stress may provide new insights into the complex mechanisms underlying waterlogging tolerance in sesame.

Keywords: LTQ-FTICR MS/MS technique, photosynthesis, protein biosynthesis, Sesamum indicum, stress defense.

Received: October 26, 2018; Revised: March 22, 2019; Accepted: March 25, 2019; Published online: November 27, 2019  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
JUNG, H.-J., ROY, S.K., CHO, S.-W., KWON, S.-J., KUN, C., CHUN, H.-C., & WOO, S.-H. (2019). Proteome analysis of sesame leaves in response to waterlogging stress at vegetative and flowering stages. Biologia plantarum63, Article 733-749. https://doi.org/10.32615/bp.2019.062
Download citation

Supplementary files

Download fileJung 5990 Suppl.pdf

File size: 1.24 MB

References

  1. Aggarwal, P.K., Kalra, N., Chander, S., Pathak, H.: InfoCrop: a dynamic simulation model for the assessment of crop yields, losses due to pests, and environmental impact of agro-ecosystems in tropical environments. I. Model description. - Agr. Syst. 89: 1-25, 2006. Go to original source...
  2. Ahmed, S., Nawata, E., Sakuratani, T.: Effects of waterlogging at vegetative and reproductive growth stages on photosynthesis, leaf water potential and yield in mungbean. - Plant Prod. Sci. 5: 117-123, 2002. Go to original source...
  3. Ahsan, N., Lee, D.-G., Lee, S.-H., Lee, K.-W., Bahk, J.D., Lee, B.-H.: A proteomic screen and identification of waterlogging-regulated proteins in tomato roots. - Plant Soil 295: 37-51, 2007a. Go to original source...
  4. Ahsan, N., Lee, D.G., Lee, S.H., Kang, K.Y., Bahk, J.D., Choi, M.S., Lee, I.J., Renaut, J., Lee, B.H.: A comparative proteomic analysis of tomato leaves in response to waterlogging stress. - Physiol Plant 131: 555-570, 2007b. Go to original source...
  5. Al-Whaibi, M.H.: Plant heat-shock proteins: a mini review. - J. King Saud Univ. Sci. 23: 139-150, 2011. Go to original source...
  6. Alam, I., Lee, D.G., Kim, K.H., Park, C.H., Sharmin, S.A., Lee, H., Oh, K.W., Yun, B.W., Lee, B.H.: Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage. - J. Biosci. 35: 49-62, 2010. Go to original source...
  7. Atkinson, N.J., Lilley, C.J., Urwin, P.E.: Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. - Plant Physiol. 162: 2028-2041, 2013. Go to original source...
  8. Bahmanyar, M.A. The influence of continuous rice cultivation and different waterlogging periods on morphology, clay mineralogy, Eh, pH, and K in paddy soils. - Pak. J. biol. Sci. 10: 2844-2849, 2007. Go to original source...
  9. Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F., Perata, P., Voesenek, L.A.C.J., Van Dongen, J.T.: Making sense of low oxygen sensing. Trends Plant Sci. 17: 129-138, 2012. Go to original source...
  10. Bailey-Serres, J., Voesenek, L.A.C.J.: Flooding stress: acclimations and genetic diversity. - Annu. Rev. Plant Biol. 59: 313-339, 2008. Go to original source...
  11. Banks, R.D., Blake, C.C., Evans, P.R., Haser, R., Rice, D.W., Hardy, G.W., Merrett, M., Phillips, A.W.: Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. - Nature 279: 773-777, 1979. Go to original source...
  12. Beckmann, R., Mizzen, L., Welch, W.: Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. - Science 248: 850-854, 1990. Go to original source...
  13. Bedigian, D.: History and lore of sesame in Southwest Asia. - Econom. Bot. 58: 330-353, 2004. Go to original source...
  14. Bian, Y.-W., Lv, D.-W., Cheng, Z.-W., Gu, A.-Q., Cao, H., Yan, Y.-M.: Integrative proteome analysis of Brachypodium distachyon roots and leaves reveals a synergetic responsive network under H2O2 stress. - J. Proteom. 128: 388-402, 2015. Go to original source...
  15. Biemelt, S., Keetman, U., Albrecht, G.: Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. - Plant Physiol. 116: 651-658, 1998. Go to original source...
  16. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  17. Chang, W.W.P., Huang, L., Shen, M., Webster, C., Burlingame, A.L., Roberts, J.K.M.: Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. - Plant Physiol. 122: 295-318, 2000. Go to original source...
  18. Chen, H., Qualls, R., Blank, R.: Effect of soil flooding on photosynthesis, carbohydrate partitioning and nutrient uptake in the invasive exotic Lepidium latifolium. - Aquat. Bot. 82: 250-268, 2005. Go to original source...
  19. Chen, Y., Chen, X., Wang, H., Bao, Y., Zhang, W.: Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. - Proteome Sci. 12: 33-33, 2014. Go to original source...
  20. Christianson, J.A., Llewellyn, D.J., Dennis, E.S., Wilson, I.W.: Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). - Plant Cell Physiol. 51: 21-37, 2010. Go to original source...
  21. Cox, M., Nelson, D.: Lehninger Principles of Biochemistry. - W.H. Freeman and Company, New York 2008.
  22. Cramer, G.R., Van Sluyter, S.C., Hopper, D.W., Pascovici, D., Keighley, T., Haynes, P.A.: Proteomic analysis indicates massive changes in metabolism prior to the inhibition of growth and photosynthesis of grapevine (Vitis vinifera L.) in response to water deficit. - BMC Plant Biol. 13: 49-49, 2013. Go to original source...
  23. Crawford, R.M.M.: Metabolic adaptation to anoxia. - In: Hook, D.D., Crawford, R.M.M. (ed.): Plant Life in Anaerobic Environments. Pp. 119-136. Ann Arbor Science, Ann Arbor 1978.
  24. Dat, J.F., Pellinen, R., Van De Cotte, B., Langebartels, C., Kangasjärvi, J., Inzé, D., Van Breusegem, F.: Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. - Plant J. 33: 621-632, 2003. Go to original source...
  25. Demirevska, K., Simova-Stoilova, L., Vassileva, V., Feller, U.: Rubisco and some chaperone protein responses to water stress and rewatering at early seedling growth of drought sensitive and tolerant wheat varieties -. Plant Growth Regul. 56: 97, 2008. Go to original source...
  26. Dossa, K., Li, D., Wang, L., Zheng, X., Liu, A., Yu, J., Wei, X., Zhou, R., Fonceka, D., Diouf, D., Liao, B.: Transcriptomic, biochemical and physio-anatomical investigations shed more light on responses to drought stress in two contrasting sesame genotypes. - Sci. Rep. 7: 8755-8755, 2017. Go to original source...
  27. Fatehi, F., Hosseinzadeh, A., Alizadeh, H., Brimavandi, T.: The proteome response of Hordeum spontaneum to salinity stress. - Cereal Res. Commun. 41: 78-87, 2013. Go to original source...
  28. Feller, U., Anders, I., Demirevska, K.: Degradation of Rubisco and other chloroplast proteins under abiotic stress. - Gen. appl. Plant Physiol. 34: 5-18, 2008.
  29. Fukao, T., Bailey-Serres, J.: Plant responses to hypoxia-is survival a balancing act? - Trends Plant Sci. 9: 449-456, 2004. Go to original source...
  30. Ghosh, D., Xu, J.: Abiotic stress responses in plant roots: a proteomics perspective. - Front. Plant Sci. 5: 6, 2014. Go to original source...
  31. He, L., Lu, X., Tian, J., Yang, Y., Li, B., Li, J., Guo, S.: Proteomic analysis of the effects of exogenous calcium on hypoxic-responsive proteins in cucumber roots. - Proteome Sci. 10: 42-42, 2012. Go to original source...
  32. Henshaw, T., Gilbert, R., Scholberg, J., Sinclair, T.: Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: II. Aboveground growth and biomass. - J. Agron. Crop Sci. 193: 189-197, 2007. Go to original source...
  33. Hoganson, C.W., Babcock, G.T.: A metalloradical mechanism for the generation of oxygen from water in photosynthesis. - Science 277: 1953-1956, 1997. Go to original source...
  34. Hossain, Z., Komatsu, S.: Potentiality of soybean proteomics in untying the mechanism of flood and drought stress tolerance. - Proteomes 2: 107-127, 2014. Go to original source...
  35. Hu, W. J., Chen, J., Liu, T.W., Wu, Q., Wang, W.H., Liu, X., Shen, Z.J., Simon, M., Wu, F.H., Pei, Z.M.: Proteome and calcium-related gene expression in Pinus massoniana needles in response to acid rain under different calcium levels. - Plant Soil 380: 285-303, 2014. Go to original source...
  36. Hu, W.J., Wu, Q., Liu, X., Shen, Z.J., Chen, J., Liu, T.W., Zhu, C.Q., Wu, F.H., Chen, L.: Comparative proteomic analysis reveals the effects of exogenous calcium against acid rain stress in Liquidambar formosana Hance leaves. - J. Proteome Res. 15: 216-228, 2015. Go to original source...
  37. Huang, H., Barker, W.C., Chen, Y., Wu, C.H.: iProClass: an integrated database of protein family, function and structure information. - Nucl. Acids Res. 31: 390-392, 2003. Go to original source...
  38. Huang, S., Greenway, H., Colmer, T.D., Millar, A.H.: Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. - Ann. Bot. 96: 703-715, 2005. Go to original source...
  39. Jansson, S.: The light-harvesting chlorophyll ab-binding proteins. - Biochim. biophys. Acta Bioenerg. 1184: 1-19, 1994. Go to original source...
  40. Kamal, A.H.M., Cho, K., Kim, D.E., Uozumi, N., Chung, K.Y., Lee, S.Y., Choi, J.S., Cho, S.W., Shin, C.S., Woo, S.H.: Changes in physiology and protein abundance in salt-stressed wheat chloroplasts. - Mol. Biol. Rep. 39: 9059-9074, 2012. Go to original source...
  41. Kanwar, S., Baker, J.L., Mukhtar, S.: Excessive soil water effects at various stages of development on the growth and yield of corn. - Trans ASAE 31: 133-0141, 1988. Go to original source...
  42. Khatoon, A., Rehman, S., Salavati, A., Komatsu, S.: A comparative proteomics analysis in roots of soybean to compatible symbiotic bacteria under flooding stress. - Amino Acids 43: 2513-2525, 2012. Go to original source...
  43. Komatsu, S., Hiraga, S., Yanagawa, Y.: Proteomics techniques for the development of flood tolerant crops. - J. Proteome Res. 11: 68-78, 2011. Go to original source...
  44. Komatsu, S., Kamal, A.H., Hossain, Z.: Wheat proteomics: proteome modulation and abiotic stress acclimation. - Front. Plant Sci. 5: 684, 2014. Go to original source...
  45. Komatsu, S., Shirasaka, N., Sakata, K.: 'Omics' techniques for identifying flooding-response mechanisms in soybean. - J. Proteom. 93: 169-178, 2013. Go to original source...
  46. Komatsu, S., Yamamoto, R., Nanjo, Y., Mikami, Y., Yunokawa, H., Sakata, K.: A comprehensive analysis of the soybean genes and proteins expressed under flooding stress using transcriptome and proteome techniques. - J. Proteome Res. 8: 4766-4778, 2009. Go to original source...
  47. Kosová, K., Práąil, I.T., Vítámvás, P.: Protein contribution to plant salinity response and tolerance acquisition. - Int. J. mol. Sci. 14: 6757-6789, 2013. Go to original source...
  48. Kosová, K., Vítámvás, P., Urban, M.O., Práąil, I.T., Renaut, J.: Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. - Front. Plant Sci. 9: 122, 2018. Go to original source...
  49. Laxalt, A.M., Cassia, R.O., Sanllorenti, P.M., Madrid, E.A., Andreu, A.B., Daleo, G.R., Conde, R.D., Lamattina, L.: Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. - Plant mol. Biol. 30: 961-972, 1996. Go to original source...
  50. Lin, K.H.R., Weng, C.C., Lo, H.F., Chen, J.T.: Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. - Plant Sci. 167: 355-365, 2004. Go to original source...
  51. Luan, H., Shen, H., Pan, Y., Guo, B., Lv, C., Xu, R.: Elucidating the hypoxic stress response in barley (Hordeum vulgare L.) during waterlogging: A proteomics approach. - Sci. Rep. 8: 9655, 2018. Go to original source...
  52. Matsumoto, M., Ogawa, K.I.: New insight into the Calvin cycle regulation-glutathionylation of fructose bisphosphate aldolase in response to illumination. - In: Allen, J.F., Gantt, E., Golbeck, J.H., Osmond, B. (ed): Photosynthesis Energy from the Sun. Pp. 871-874. Springer, Dordrecht 2008. Go to original source...
  53. Mishra, S., Patro, L., Mohapatra, P., Biswal, B.: Response of senescing rice leaves to flooding stress. - Photosynthetica 46: 315, 2008. Go to original source...
  54. Mustafa, G., Komatsu, S.: Quantitative proteomics reveals the effect of protein glycosylation in soybean root under flooding stress. - Front. Plant Sci. 5: 627, 2014. Go to original source...
  55. Nakano, R., Ishida, H., Kobayashi, M., Makino, A., Mae, T.: Biochemical changes associated with in vivo RbcL fragmentation by reactive oxygen species under chilling-light conditions. - Plant Biol. 12: 35-45, 2010. Go to original source...
  56. Nakashima, K., Ito, Y., Yamaguchi-Shinozaki, K.: Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. - Plant Physiol. 149: 88-95, 2009. Go to original source...
  57. Nanjo, Y., Maruyama, K., Yasue, H., Yamaguchi-Shinozaki, K., Shinozaki, K., Komatsu, S.: Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. - Plant mol. Biol. 77: 129-144, 2011. Go to original source...
  58. Ndimba, B.K., Chivasa, S., Simon, W.J., Slabas, A.R.: Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. - Proteomics 5: 4185-4196, 2005. Go to original source...
  59. Neill, S., Desikan, R., Hancock, J.: Hydrogen peroxide signalling. - Curr. Opin. Plant Biol. 5: 388-395, 2002. Go to original source...
  60. Ngamhui, N.-O., Akkasaeng, C., Zhu, Y.J., Tantisuwichwong, N., Roytrakul, S., Sansayawichai, T.: Differentially expressed proteins in sugarcane leaves in response to water deficit stress. - Plant Omics 5: 365, 2012.
  61. O'Farrell, P.H.: High resolution two-dimensional electrophoresis of proteins. - J. biol. Chem. 250: 4007-4021, 1975. Go to original source...
  62. Pociecha, E., Ko¶cielniak, J., Filek, W.: Effects of root flooding and stage of development on the growth and photosynthesis of field bean (Vicia faba L. minor). - Acta Physiol. Plant. 30: 529, 2008. Go to original source...
  63. Qi, X.H., Xu, X.W., Lin, X.J., Zhang, W.J., Chen, X.H.: Identification of differentially expressed genes in cucumber (Cucumis sativus L.) root under waterlogging stress by digital gene expression profile. - Genomics 99: 160-168, 2012. Go to original source...
  64. Qureshi, M.I., Qadir, S., Zolla, L.: Proteomics-based dissection of stress-responsive pathways in plants. - J. Plant Physiol. 164: 1239-1260, 2007. Go to original source...
  65. Ram, R., Catlin, D., Romero, J., Cowley, C.: Sesame: new approaches for crop improvemen.t - In: Janick, J., Simon, J.E. (ed.):: Advances in New Crops. Pp. 225-228. Timber Press, Portland 1990.
  66. Reicosky, D., Meyer, W., Schaefer, N., Sides, R.: Cotton response to short-term waterlogging imposed with a water-table gradient facility. - Agr. Water Manage. 10: 127-143, 1985. Go to original source...
  67. Rogalski, M., Schöttler, M.A., Thiele, W., Schulze, W.X., Bock, R.: Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. - Plant Cell 20: 2221-2237, 2008. Go to original source...
  68. Roy, S.K., Kwon, S.J., Cho, S.W., Kamal, A.H.M., Kim, S.W., Sarker, K., Oh, M.W., Lee, M.S., Chung, K.Y., Xin, Z.: Leaf proteome characterization in the context of physiological and morphological changes in response to copper stress in sorghum. - BioMetals 29: 495-513, 2016. Go to original source...
  69. Sachs, M.M., Subbaiah, C.C., Saab, I.N.: Anaerobic gene expression and flooding tolerance in maize. - J. exp. Bot. 47: 1-15, 1996. Go to original source...
  70. Saha, R., Ahmed, F., Mokarroma, N., Rohman, M., Golder, P.: Physiological and biochemical changes in waterlogging tolerant sesame genotypes. - SAARC J. Agr. 14: 31-45, 2016. Go to original source...
  71. Sairam, R., Kumutha, D., Ezhilmathi, K., Chinnusamy, V., Meena, R.: Waterlogging induced oxidative stress and antioxidant enzyme activities in pigeon pea. - Biol. Plant. 53: 493-504, 2009. Go to original source...
  72. Sairam, R.K., Dharmar, K., Lekshmy, S., Chinnusamy, V.: Expression of antioxidant defense genes in mung bean (Vigna radiata L.) roots under water-logging is associated with hypoxia tolerance -. Acta Physiol. Plant. 33: 735-744, 2011. Go to original source...
  73. Sang, Q., Shan, X., An, Y., Shu, S., Sun, J., Guo, S.: Proteomic analysis reveals the positive effect of exogenous spermidine in tomato seedlings' response to high-temperature stress. - Front. Plant Sci. 8: 120, 2017. Go to original source...
  74. Shabala, S.: Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. - New Phytol. 190: 289-298, 2011. Go to original source...
  75. Sharma, D., Swarup, A.: Effects of short-term flooding on growth, yield and mineral composition of wheat on sodic soil under field conditions. - Plant Soil 107: 137-143, 1988. Go to original source...
  76. Shi, J., Chen, Y., Xu, Y., Ji, D., Chen, C., Xie, C.: Differential proteomic analysis by iTRAQ reveals the mechanism of Pyropia haitanensis responding to high temperature stress. - Sci. Rep. 7: 44734, 2017. Go to original source...
  77. Spreitzer, R.J., Salvucci, M.E.: Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. - Annu. Rev. Plant Biol. 53:449-475, 2002. Go to original source...
  78. Staneloni, R.J., Rodriguez-Batiller, M.J., Casal, J.J.: Abscisic acid, high-light, and oxidative stress down-regulate a photosynthetic gene via a promoter motif not involved in phytochrome-mediated transcriptional regulation. - Mol. Plant 1: 75-83, 2008. Go to original source...
  79. Stoychev, V., Simova-Stoilova, L., Vaseva, I., Kostadinova, A., Nenkova, R., Feller, U., Demirevska, K.: Protein changes and proteolytic degradation in red and white clover plants subjected to waterlogging. - Acta Physiol. Plant. 35: 1925-1932, 2013. Go to original source...
  80. Subbaiah, C.C., Sachs, M.M.: Molecular and cellular adaptations of maize to flooding stress. - Ann. Bot. 91: 119-127, 2003. Go to original source...
  81. Sun, J., Zhang, X., Zhang, Y., Wang, L., Huang, B.: Effects of waterlogging on leaf protective enzyme activities and seed yield of sesame at different growth stages. - Chin. J. appl. environ. Biol. 15: 790-795, 2009. Go to original source...
  82. Tamburino, R., Vitale, M., Ruggiero, A., Sassi, M., Sannino, L., Arena, S., Costa, A., Batelli, G., Zambrano, N., Scaloni, A.: Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). - BMC Plant Biol. 17: 40, 2017. Go to original source...
  83. Thirunavukkarasu, N., Hossain, F., Mohan, S., Shiriga, K., Mittal, S., Sharma, R., Singh, R.K., Gupta, H.S.: Genome-wide expression of transcriptomes and their co-expression pattern in subtropical maize (Zea mays L.) under waterlogging stress. - PLoS ONE 8: e70433, 2013. Go to original source...
  84. Vassileva, V., Demirevska, K., Simova-Stoilova, L., Petrova, T., Tsenov, N., Feller, U.: Winter wheat cultivars under long-term field drought-biochemical and ultrastructural constraints affecting yield. - J. Agron. Crop Sci. 198: 104-117, 2011. Go to original source...
  85. Wang, D., Pan, Y., Zhao, X., Zhu, L., Fu, B., Li, Z.: Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. - BMC Genomics 12: 149, 2011. Go to original source...
  86. Wang, L., Li, D., Zhang, Y., Gao, Y., Yu, J., Wei, X., Zhang, X.: Tolerant and susceptible sesame genotypes reveal waterlogging stress response patterns. - PLoS ONE 11: e0149912, 2016a. Go to original source...
  87. Wang, L., Zhang, Y., Qi, X., Li, D., Wei, W., Zhang, X.: Global gene expression responses to waterlogging in roots of sesame (Sesamum indicum L.). - Acta Physiol. Plant. 34: 2241-2249, 2012. Go to original source...
  88. Wang, N., Zhao, J., He, X., Sun, H., Zhang, G., Wu, F.: Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. - BMC Genomics 16: 432, 2015. Go to original source...
  89. Wang, W., Vinocur, B., Shoseyov, O., Altman, A.: Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. - Trends Plant Sci. 9: 244-252, 2004. Go to original source...
  90. Wang, X., Deng, Z., Zhang, W., Meng, Z., Chang, X., Lv, M.: Effect of waterlogging duration at different growth stages on the growth, yield and quality of cotton. - PLoS ONE 12: e0169029: 2017. Go to original source...
  91. Wang, X., Huang, M., Zhou, Q., Cai, J., Dai, T., Cao, W., Jiang, D.: Physiological and proteomic mechanisms of waterlogging priming improves tolerance to waterlogging stress in wheat (Triticum aestivum L.). - Environ. exp. Bot. 132: 175-182, 2016b. Go to original source...
  92. Wang, Z.Y., Portis, A.R.: Dissociation of ribulose-1,5-bisphosphate bound to ribulose-1,5-bisphosphate carboxylase/oxygenase and its enhancement by ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated hydrolysis of ATP. - Plant Physiol. 99: 1348-1353, 1992. Go to original source...
  93. Weger, H.G., Turpin, D.H.: Mitochondrial respiration can support NO3- and NO2- reduction during photosynthesis: interactions between photosynthesis, respiration, and N assimilation in the N-limited green alga Selenastrum minutum. - Plant Physiol. 89: 409-415, 1989. Go to original source...
  94. Wei, W., Li, D., Wang, L., Ding, X., Zhang, Y., Gao, Y., Zhang, X.: Morpho-anatomical and physiological responses to waterlogging of sesame (Sesamum indicum L.). - Plant Sci. 208: 102-111, 2013. Go to original source...
  95. Whittle, C.A., Krochko, J.E.: Transcript profiling provides evidence of functional divergence and expression networks among ribosomal protein gene paralogs in Brassica napus. - Plant Cell 21: 2203-2219, 2009. Go to original source...
  96. Won Oh, M., Nanjo, Y., Komatsu, S.: Identification of nuclear proteins in soybean under flooding stress using proteomic technique. - Protein Peptide Lett. 21: 458-467, 2014. Go to original source...
  97. Xu, X., Ji, J., Ma, X., Xu, Q., Qi, X., Chen, X.: Comparative proteomic analysis provides insight into the key proteins involved in cucumber (Cucumis sativus L.) adventitious root emergence under waterlogging stress. - Front Plant Sci. 7: 1515, 2016. Go to original source...
  98. Yamauchi, T., Watanabe, K., Fukazawa, A., Mori, H., Abe, F., Kawaguchi, K., Oyanagi, A., Nakazono, M. Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. - J. exp. Bot. 65: 261-273, 2014. Go to original source...
  99. Yang, S.F., Hoffman, N.E.: Ethylene biosynthesis and its regulation in higher plants. - Annu. Rev. Plant Physiol. 35: 155-189, 1984. Go to original source...
  100. Yao, Y.-X., Li, M., Zhai, H., You, C.-X., and Hao, Y.-J.: Isolation and characterization of an apple cytosolic malate dehydrogenase gene reveal its function in malate synthesis. - J. Plant Physiol. 168: 474-480, 2011. Go to original source...
  101. Yu, F., Han, X., Geng, C., Zhao, Y., Zhang, Z., Qiu, F.: Comparative proteomic analysis revealing the complex network associated with waterlogging stress in maize (Zea mays L.) seedling root cells -. Proteomics 15: 135-147, 2015. Go to original source...
  102. Zhai, L., Liu, Z., Zou, X., Jiang, Y., Qiu, F., Zheng, Y., Zhang, Z.: Genome-wide identification and analysis of microRNA responding to long-term waterlogging in crown roots of maize seedlings. - Physiol. Plant 147: 181-193, 2013. Go to original source...
  103. Zhu, X., Li, X., Jiu, S., Zhang, K., Wang, C., Fang, J.: Analysis of the regulation networks in grapevine reveals response to waterlogging stress and candidate gene-marker selection for damage severity. - Royal Soc. Open Sci. 5: 172253, 2018. Go to original source...
  104. Zou, X., Jiang, Y., Liu, L., Zhang, Z., Zheng, Y.: Identification of transcriptome induced in roots of maize seedlings at the late stage of waterlogging. - BMC Plant Biol. 10: 189, 2010. Go to original source...
  105. Zou, X., Tan, X., Hu, C., Zeng, L., Lu, G., Fu, G., Cheng, Y., Zhang, X.: The transcriptome of Brassica napus L. roots under waterlogging at the seedling stage. - Int. J. mol. Sci. 14: 2637-2651, 2013. Go to original source...