Photosynthetica 2020, 58(3):780-789 | DOI: 10.32615/ps.2020.027

Photosynthetic response and transcriptomic profiling provide insights into the alkali tolerance of clone halophyte Leymus chinensis

H. WANG1, Y. XIANG1, L.H. LI2, N. BHANBHRO2, C.W. YANG2, Z. ZHANG1
1 Department of Agronomy, Jilin Agricultural University, 130118 Changchun, China
2 Key Laboratory of Molecular Epigenetics of Ministry of Education, Northeast Normal University, 130024 Changchun, China

Alkali stress is one of the important factors in restricting agriculture production. Leymus chinensis is constructive halophyte species in alkalized grassland in China. In order to investigate the gene expression response of L. chinensis to alkali stress, we used PacBio technology to obtain reference full-length transcript sequences for transcriptomic analysis of alkali stress response. In order to elucidate the alkali tolerance mechanisms of L. chinensis, we measured the photosynthetic parameters, concentrations of ions and compatible solutes, chloroplast ultrastructure and anatomy of control and stressed plants. Our results showed that L. chinensis shares many alkali-tolerance mechanisms with glycophytes. Higher stability of photosynthetic apparatus under alkali stress may be prominent alkali-tolerance trait of L. chinensis. L. chinensis may have a strong capacity to decline the toxicity of Na+ to organelles and cytoplasmic proteins. Enhanced expression of dehydrin and LEA genes and increased accumulation of carbohydrates may contribute to the development of Na+-specific stress tolerance of L. chinensis under alkali stress.

Additional key words: osmotic adjustment; PacBio sequencing; pigments; RNAseq.

Received: December 27, 2019; Revised: March 12, 2020; Accepted: March 19, 2020; Prepublished online: May 15, 2020; Published: June 11, 2020  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
WANG, H., XIANG, Y., LI, L.H., BHANBHRO, N., YANG, C.W., & ZHANG, Z. (2020). Photosynthetic response and transcriptomic profiling provide insights into the alkali tolerance of clone halophyte Leymus chinensis. Photosynthetica, 58(3), 780-789. doi: 10.32615/ps.2020.027
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileWang 2505 supplement - Table 7S.xlsx

    File size: 10.07 kB

    Download fileWang 2505 supplement - Table 6S.xlsx

    File size: 13.46 kB

    Download fileWang 2505 supplement - Table 5S.xls

    File size: 210 kB

    Download fileWang 2505 supplement - Table 2S.xlsx

    File size: 8.51 kB

    Download fileWang 2505 supplement - Table 1S.xlsx

    File size: 9.96 kB

    Download fileWang 2505 supplement - Table 3S.xlsx

    File size: 5.06 MB

    Download fileWang 2505 supplement - Table 4S.xlsx

    File size: 5.43 MB

    References

    1. Abdelraheem A., Esmaeili N., O'Connell M., Zhang J.: Progress and perspective on drought and salt stress tolerance in cotton. - Ind. Crop. Prod. 130: 118-129, 2019. Go to original source...
    2. Ardie S.W., Liu S.K., Takano T.: Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis. - Plant Cell Rep. 29: 865-874, 2010. Go to original source...
    3. Ardie S.W., Nishiuchi S., Liu S.K., Takano T.: Ectopic expression of the channel β subunits from Puccinellia tenuiflora (KPutB1) and rice (KOB1) alters K+/Na+ homeostasis of yeast and Arabidopsis. - Mol. Biotechnol. 48: 76-86, 2011. Go to original source...
    4. Ardie S.W., Xie L., Takahashi R. et al.: Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis. - J. Exp. Bot. 60: 3491-3502, 2009. Go to original source...
    5. Buitink J., Leprince O.: Intracellular glasses and seed survival in the dry state. - C. R. Biol. 331: 788-795, 2008. Go to original source...
    6. Crawford N.M., Glass A.D.M.: Molecular and physiological aspects of nitrate uptake in plants. - Trends Plant Sci. 10: 389-395, 1998. Go to original source...
    7. Flowers T.J, Yeo A.R.: Breeding for salinity resistance in crop plants: Where next? - Aust. J. Plant Physiol. 22: 875-884, 1995. Go to original source...
    8. Flowers T.J., Galal H.K., Bromham L.: Evolution of halophytes: multiple origins of salt tolerance in land plants. - Funct. Plant Biol. 37: 604-612, 2010. Go to original source...
    9. Flowers T.J., Glenn E.P., Volkov V.: Could vesicular transport of Na+ and Cl- be a feature of salt tolerance in halophytes? - Ann. Bot.-London 123: 1-18, 2019. Go to original source...
    10. Ganie S.A., Molla K.A., Henry R.J. et al.: Advances in understanding salt tolerance in rice. - Theor. Appl. Genet. 132: 851-870, 2019. Go to original source...
    11. Guo R., Shi L., Yang C. et al.: Comparison of ionomic and metabolites response under alkali stress in old and young leaves of cotton (Gossypium hirsutum L.) seedlings. - Front. Plant Sci. 7: 1785, 2016. Go to original source...
    12. He R., Yu G., Han X. et al.: ThPP1 gene, encodes an inorganic pyrophosphatase in Thellungiella halophila, enhanced the tolerance of the transgenic rice to alkali stress. - Plant Cell Rep. 36: 1929-1942, 2017. Go to original source...
    13. Jia X.M., Wang H., Sofkova S. et al.: Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. - Sci. Hortic.-Amsterdam 245:154-162, 2019. Go to original source...
    14. Jin H., Kim H.R., Plaha P. et al.: Expression profiling of the genes induced by Na2CO3 and NaCl stresses in leaves and roots of Leymus chinensis. - Plant Sci. 175: 784-792, 2008. Go to original source...
    15. Kaashyap M., Ford R., Bohra A. et al.: Improving salt tolerance of chickpea using modern genomics tools and molecular breeding. - Curr. Genomics 18: 557-567, 2017. Go to original source...
    16. Li R., Shi F., Fukuda K.: Interactive effects of various salt and alkali stresses on growth, organic solutes, and cation accumulation in a halophyte Spartina alterniflora (Poaceae). -Environ. Exp. Bot. 68: 66-74, 2010. Go to original source...
    17. Liu B., Kang C., Wang X., Bao G.: Physiological and morphological responses of Leymus chinensis to saline-alkali stress. - Grassl. Sci. 61: 217-226, 2015. Go to original source...
    18. Liu H., Zhang X.X., Takano T., Liu S.K.: Characterization of a PutCAX1 gene from Puccinellia tenuiflora that confers Ca2+ and Ba2+ tolerance in yeast. - Biochem. Bioph. Res. Co. 383: 392-396, 2009. Go to original source...
    19. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
    20. Ma Y., Wang X.-P., Jiang H.-B., Shi D.-C.: Characteristics of organic acids accumulation and oxalate metabolism in Kochia sieversiana under salt and alkali stresses. - Acta Pratacult. Sin. 26: 158-165, 2017.
    21. Munns R., Gilliham M.: Salinity tolerance of crops - what is the cost? - New Phytol. 208: 668-673, 2015. Go to original source...
    22. Munns R., Tester M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
    23. Rorat T.: Plant dehydrins - tissue location, structure and func-tion. - Cell Mol. Biol. Lett. 11: 536-556, 2006. Go to original source...
    24. Rozentsvet O.A., Nesterov V.N., Bogdanova E.S.: Structural, physiological, and biochemical aspects of salinity tolerance of halophytes. - Russ. J. Plant Physl+ 64: 464-477, 2017. Go to original source...
    25. Shi W., Xu W., Li S. et al.: Responses of two rice cultivars differing in seedling-stage nitrogen use efficiency to growth under low-nitrogen conditions. - Plant Soil 326: 291-302, 2009. Go to original source...
    26. Tanji K.K.E.: Agricultural Salinity Assessment and Management. Pp. 112. American Society of Civil Engineers, New York 1990.
    27. Wang F., Chen Z.H., Liu X. et al.: The loss of RBOHD function modulates root adaptive responses to combined hypoxia and salinity stress in Arabidopsis. - Environ. Exp. Bot. 158: 125-135, 2019. Go to original source...
    28. Wang F.W., Wang C., Sun Y. et al.: Overexpression of vacuolar proton pump ATPase (V-H+-ATPase) subunits B, C and H confers tolerance to salt and saline-alkali stresses in transgenic alfalfa (Medicago sativa L.). - J. Integr. Agr. 15: 2279-2289, 2016. Go to original source...
    29. Wang H., Ahan J., Wu Z. et al.: Alteration of nitrogen metabolism in rice variety 'Nipponbare' induced by alkali stress. - Plant Soil 355: 131-147, 2012. Go to original source...
    30. Wang H., Lin X., Cao S., Wu Z.: Alkali tolerance in rice (Oryza sativa L.): growth, photosynthesis, nitrogen metabolism, and ion homeostasis. - Photosynthetica 53: 55-65, 2015. Go to original source...
    31. Wang L., Fang C., Wang K.: Physiological responses of Leymus chinensis to long-term salt, alkali and mixed salt-alkali stresses. - J. Plant Nutr. 38: 526-540, 2015. Go to original source...
    32. Wang M., Xia G.: The landscape of molecular mechanisms for salt tolerance in wheat. - Crop J. 6: 42-47, 2018. Go to original source...
    33. Wang P., Cui Y.N., Gao L., Wang S.M.: Construction of RNAi expression vector of CYP86A gene in halophyte Puccinellia tenuiflora. - Acta Pratacult. Sin. 26: 105-110, 2017. [In Chinese]
    34. Wang Y., Chu Y., Liu G. et al.: Identification of expressed sequence tags in an alkali grass (Puccinellia tenuiflora) cDNA library. - J. Plant Physiol. 164: 78-89, 2007. Go to original source...
    35. Wang Y., Yang C., Liu G., Jiang J.: Development of a cDNA microarray to identify gene expression of Puccinellia tenuiflora under saline-alkali stress. - Plant Physiol. Bioch. 45: 567-576, 2007. Go to original source...
    36. Wu H., Shabala L., Azzarello E.: Na+ extrusion from the cytosol and tissue-specific Na+ sequestration in roots confer differential salt stress tolerance between durum and bread wheat. - J. Exp. Bot. 69: 3987-4001, 2018. Go to original source...
    37. Yang C., Shi D., Wang D.: Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). - Plant Growth Regul. 56: 179, 2008a. Go to original source...
    38. Yang C., Chong J., Li C. et al.: Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. - Plant Soil 294: 263-276, 2007. Go to original source...
    39. Yang C., Wang P., Li C. et al.: Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. - Photosynthetica 46: 107-114, 2008b. Go to original source...
    40. Yin Z., Zhang H., Zhao Q. et al.: Physiological and comparative proteomic analyses of saline-alkali NaHCO3-responses in leaves of halophyte Puccinellia tenuiflora. - Plant Soil 437: 137-158, 2019. Go to original source...
    41. Yu J.J., Chen S.X., Wang T. et al.: Comparative proteomic analysis of Puccinellia tenuiflora leaves under Na2CO3 stress. - Int. J. Mol. Sci. 14: 1740-1762, 2013. Go to original source...
    42. Yu J.J., Chen S.X., Zhao Q. et al.: Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. - J. Proteome Res. 10: 3852-3870, 2011. Go to original source...
    43. Zeng Y., Li Q., Wang H. et al.: Two NHX-type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress. - Plant Biotechnol. J. 16: 310-321, 2018. Go to original source...
    44. Zhai J., Dong Y., Sun Y. et al.: Discovery and analysis of microRNAs in Leymus chinensis under saline-alkali and drought stress using high-throughput sequencing. - PLoS ONE 9: e105417, 2014. Go to original source...
    45. Zhang A., Zang W., Zhang X. et al.: Global proteomic mapping of alkali stress regulated molecular networks in Helianthus tuberosus L. - Plant Soil 409: 175-202, 2016. Go to original source...
    46. Zhang W.-D., Wang P., Bao Z. et al.: SOS1, HKT1;5, and NHX1 synergistically modulate Na+ homeostasis in the halophytic grass Puccinellia tenuiflora. - Front. Plant Sci. 8: 576, 2017. Go to original source...
    47. Zhang M., Cao Y., Wang Z. et al.: A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize. - New Phytol. 217: 1161-1176, 2018. Go to original source...
    48. Zhang X., Wei L., Wang Z., Wang T.: Physiological and molecular features of Puccinellia tenuiflora tolerating salt and alkaline-salt stress. - J. Integr. Plant Biol. 55: 262-276, 2013. Go to original source...
    49. Zhao L., Yang Z., Yang C.: Transcriptomic profiling and physiological responses of halophyte Kochia sieversiana provide insights into salt tolerance. - Front. Plant Sci. 8: 1985, 2017. Go to original source...
    50. Zhao Z., Liu J., Jia R. et al.: Physiological and TMT-based proteomic analysis of oat early seedlings in response to alkali stress. - J. Proteomics 193: 10-26, 2019. Go to original source...
    51. Zheng H.Y., Li J.D.: [Form and dynamic trait of halophyte community.] - In: Zheng H.Y., Li J.D. (ed.): [Saline Plants in Songnen Plain and Restoration of Alkaline-Saline Grass.] Pp. 137-138. Science Press, Beijing 1999. [In Chinese]
    52. Zhu D., Hou L., Xiao P. et al.: VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. - Plant Sci. 280: 132-142, 2019. Go to original source...
    53. Zhu G.L.: Carotenoid and chlorophyll determination. - In: Zhu G.L. (ed.): [Laboratory Manual of Plant Physiology.] Pp. 51-54. Beijing University Press, Beijing 1993. [In Chinese]

    Return to the content