biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 67:114-125, 2023 | DOI: 10.32615/bp.2023.009

Transcriptome analysis shows that alkalinity affects metabolism in the roots of Mesembryanthemum crystallinum

Y.X. Hei1, J. Liu1, *, Z.X. Zhang2, J.Y. Jiang1, S.H. Yu3, Z.Z. Zhu4, M. Mi5
1 Institute of Horticulture Research, Taizhou Academy of Agricultural Sciences, Taizhou 317000, P.R. China
2 School of Accounting, Zhejiang University of Finance and Economics, Hangzhou, 310018, P.R. China
3 Institute of Ecology Research, Taizhou Academy of Agricultural Sciences, Taizhou 317000, P.R. China
4 Institute of Vegetable Research, Taizhou Academy of Agricultural Sciences, Taizhou 317000, P.R. China
5 Institute of Biological Technology Research, Taizhou Academy of Agricultural Sciences, Taizhou 317000, P.R. China

Mesembryanthemum crystallinum is a model halophyte that switches from C3 photosynthesis to Crassulacean acid metabolism (CAM) upon extreme abiotic stresses. This study aimed to investigate alkalinity-induced root transcriptome profiling in M. crystallinum. M. crystallinum seedlings were treated with 50 mM sodium bicarbonate (NaHCO3; pH 7.5) and 90 mM NaHCO3 (pH 9.5) for 7 d, respectively. Alkalinity-induced differentially expressed genes (DEGs) were identified and annotated. Functional enrichment analysis was performed for DEGs. The expression of genes related to response to stress and CAM were analyzed and compared. Comparing with control, 50 and 90 mM NaHCO3 treatments induced 4 027 and 25 403 DEGs in M. crystallinum roots, respectively. Among these DEGs, 832 and 131 DEGs were consistently upregulated and downregulated by both stresses, respectively. These genes were associated with multiple biological processes related to response to abiotic stresses. Alkaline stress upregulated genes encoding heat shock proteins and ethylene-related genes, but downregulated genes encoding glutathione S-transferases. Also, genes that encode phosphoenolpyruvate carboxylases, phosphoenolpyruvate carboxylase kinase 1, and malate dehydrogenases related to malate accumulation were upregulated by alkalinity. This study indicated that alkaline stress affected the genes related to stress responses, metabolism, and malate accumulation in the roots of M. crystallinum.

Keywords: alkalinity tolerance, Crassulacean acid metabolism, DEGs, ice plant, Mesembryanthemum crystallinum, NaHCO3, phosphoenolpyruvate carboxylase.

Received: January 28, 2022; Revised: February 13, 2023; Accepted: March 30, 2023; Published online: June 15, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Hei, Y.X., Liu, J., Zhang, Z.X., Jiang, J.Y., Yu, S.H., Zhu, Z.Z., & Mi, M. (2023). Transcriptome analysis shows that alkalinity affects metabolism in the roots of Mesembryanthemum crystallinum. Biologia plantarum, 67, Article 114-125. https://doi.org/10.32615/bp.2023.009
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 file6854_Hei_Suppl.pdf

    File size: 2.06 MB

    Download file6854_Hei_Suppl_Table_3_Suppl.xlsx

    File size: 192.51 kB

    Download file6854_Hei_Suppl_Table_4_Suppl.xlsx

    File size: 41.92 kB

    References

    1. Adams R.P., Peña F., Wilcox E., Scow B.: The effects extreme alkaline soil on biomass and hydrocarbon yields in Helianthus annuus cv. Munchkin, Firecracker and Little Becka (Asteraceae, sunflowers). - Phytologia 102: 143-149, 2020.
    2. Bai L., Wang C., Zang S. et al.: Remote sensing of soil alkalinity and salinity in the Wuyu'er-Shuangyang River Basin, Northeast China. - Remote Sens. 8: 163, 2016. Go to original source...
    3. Barkla B.J., Vera-Estrella R., Raymond C.: Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins. - BMC Plant Biol. 16: 110, 2016. Go to original source...
    4. Bohnert H.J., Cushman J.C.: The ice plant cometh: lessons in abiotic stress tolerance. - J. Plant Growth Regul. 19: 334-346, 2000. Go to original source...
    5. Byun M.Y., Cui L.H., Lee J. et al.: Identification of rice genes associated with enhanced cold tolerance by comparative transcriptome analysis with two transgenic rice plants overexpressing DaCBF4 or DaCBF7, isolated from Antarctic flowering plant Deschampsia antarctica. - Front. Plant Sci. 9: 601, 2018. Go to original source...
    6. Chiang C.-P., Yim W.C., Sun Y.-H. et al.: Identification of ice plant (Mesembryanthemum crystallinum L.) microRNAs using RNA-Seq and their putative roles in high salinity responses in seedlings. - Front. Plant Sci. 7: 1143, 2016. Go to original source...
    7. Choi J.-H., Jo S.-G., Jung S.-K. et al.: Immunomodulatory effects of ethanol extract of germinated ice plant (Mesembryanthemum crystallinum). - Lab. Animal Res. 33: 32-39, 2017. Go to original source...
    8. Cushman J.C., Tillett R.L., Wood J.A. et al.: Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photo­synthesis and Crassulacean acid metabolism (CAM). - J. Exp. Bot. 59: 1875-1894, 2008. Go to original source...
    9. Dixit V.K., Misra S., Mishra S.K. et al.: Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays. - Anton. Leeuw. 113: 889-905, 2020. Go to original source...
    10. Doubnerová V., Ry¹lavá H.: What can enzymes of C₄ photosynthesis do for C₃ plants under stress? - Plant Sci. 180: 575-583, 2011. Go to original source...
    11. Ewe D., Tachibana M., Kikutani S. et al.: The intracellular distribution of inorganic carbon fixing enzymes does not support the presence of a C4 pathway in the diatom Phaeodactylum tricornutum. - Photosynth. Res. 137: 263-280, 2018. Go to original source...
    12. Food and Nations AOotU.: Extent and causes of salt-affected soils in participating countries. Global network on integrated soil management for sustainable use of salt-affected soils. FAO Land and Plant Nutrition Management Service, Rome 2000.
    13. Gautam R., Meena R.K., Woch N., Kirti P.: Ectopic expression of BrALDH7B2 gene encoding an antiquitin from Brassica rapa confers tolerance to abiotic stresses and improves photosynthetic performance under salt stress in tobacco. - Environ. Exp. Bot. 180: 104223, 2020. Go to original source...
    14. Ghangal R., Rajkumar M.S., Garg R., Jain M.: Genome-wide analysis of glutathione S-transferase gene family in chickpea suggests its role during seed development and abiotic stress. - Mol. Biol. Rep. 47: 2749-2761, 2020. Go to original source...
    15. Gil-Monreal M., Zabalza A., Missihoun T.D. et al.: Induction of the PDH bypass and upregulation of the ALDH7B4 in plants treated with herbicides inhibiting amino acid biosynthesis. - Plant Sci. 264: 16-28, 2017. Go to original source...
    16. Grabherr M.G., Haas B.J., Yassour M. et al.: Full-length transcriptome assembly from RNA-Seq data without a reference genome. - Nat. Biotechnol. 29: 644-662, 2011. Go to original source...
    17. Guan Q., Tan B., Kelley T.M. et al.: Physiological changes in Mesembryanthemum crystallinum during the C3 to CAM transition induced by salt stress. - Front. Plant Sci. 11: 283, 2020. Go to original source...
    18. Hasan M.S., Islam S., Hasan M.N. et al.: Genome-wide analysis and transcript profiling identify several abiotic and biotic stress-responsive glutathione S-transferase genes in soybean. - Plant Gene 23: 100239, 2020. Go to original source...
    19. He J., Chua E.L., Qin L.: Drought does not induce crassulacean acid metabolism (CAM) but regulates photosynthesis and enhances nutritional quality of Mesembryanthemum crystallinum. - PLoS ONE 15: e0229897, 2020. Go to original source...
    20. Hsieh E.-J., Waters B.M.: Alkaline stress and iron deficiency regulate iron uptake and riboflavin synthesis gene expression differently in root and leaf tissue: implications for iron deficiency chlorosis. - J. Exp. Bot. 67: 5671-5685, 2016. Go to original source...
    21. Khan A.R., Wakeel A., Muhammad N. et al.: Involvement of ethylene signaling in zinc oxide nanoparticle-mediated biochemical changes in Arabidopsis thaliana leaves. - Environ. Sci.-Nano 6: 341-355, 2019. Go to original source...
    22. Kholodova V., Volkov K., Abdeyeva A., Kuznetsov V.: Water status in Mesembryanthemum crystallinum under heavy metal stress. - Environ. Exp. Bot. 71: 382-389, 2011. Go to original source...
    23. Kong W., Yoo M.J., Zhu D. et al.: Molecular changes in Mesembryanthemum crystallinum guard cells underlying the C3 to CAM transition. - Plant Mol. Biol. 103: 653-667, 2020. Go to original source...
    24. Kong X., Tian H., Yu Q. et al.: PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. - Cell Rep. 22: 1350-1363, 2018. Go to original source...
    25. Kumar S., Trivedi P.K.: Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. - Front. Plant Sci. 9: 751, 2018. Go to original source...
    26. Kustka A.B., Milligan A.J., Zheng H. et al.: Low CO2 results in a rearrangement of carbon metabolism to support C4 photosynthetic carbon assimilation in Thalassiosira pseudonana. - New Phytol. 204: 507-520, 2014. Go to original source...
    27. Ku¼niak E., Kornas A., Ka¼mierczak A. et al.: Photosynthesis-related characteristics of the midrib and the interveinal lamina in leaves of the C3-CAM intermediate plant Mesembryanthemum crystallinum. - Ann. Bot.-London 117: 1141-1151, 2016. Go to original source...
    28. Li J., Xu H.-H., Liu W.-C. et al.: Ethylene inhibits root elongation during alkaline stress through AUXIN1 and associated changes in auxin accumulation. - Plant Physiol. 168: 1777-1791, 2015. Go to original source...
    29. Lin Y.-H., Kuo W.-W., Chen I.-H. et al.: Uses of Mesembryanthemum crystallinum L. callus extract in delaying skin cell aging, nursing skin, treating and preventing skin cancer. United States Patent Application No. US 2017/0274029 A1. Available at: https://www.freepatentsonline.com/y2017/0274029.html, 2020.
    30. Liu X., Li X., Zhang C. et al.: Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress. - Physiol. Plantarum 159: 178-200, 2017. Go to original source...
    31. Ma H.: Saline-alkaline resistance: physiological and ecological characteristics of sheepgrass (Leymus chinensis). - In: Liu G., Li X., Zhang Q. (ed.): Sheepgrass (Leymus chinensis): An Environmentally Friendly Native Grass for Animals. Pp. 117-137. Springer, Singapore 2019. Go to original source...
    32. Ma Q., Jin K., Peng G., Xia Y.: An ENA ATPase, MaENA1, of Metarhizium acridum influences the Na+-, thermo- and UV-tolerances of conidia and is involved in multiple mechanisms of stress tolerance. - Fungal Genet. Biol. 83: 68-77, 2015. Go to original source...
    33. Mishra D., Shekhar S., Singh D. et al.: Heat shock proteins and abiotic stress tolerance in plants. - In: Asea A., Kaur P. (ed.): Regulation of Heat Shock Protein Responses. Heat Shock Proteins. Vol. 13. Pp. 41-69. Springer, Cham 2018. Go to original source...
    34. Oh D.H., Barkla B.J., Vera-Estrella R. et al.: Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum. - New Phytol. 207: 627-644, 2015. Go to original source...
    35. Okur B., Örçen N.: Soil salinization and climate change. - In: Prasad M.N.V., Pietrzykowski M. (ed.): Climate Change and Soil Interactions. Pp. 331-350. Elsevier, Amsterdam 2020. Go to original source...
    36. Ostrem J.A., Olson S.W., Schmitt J.M., Bohnert H.J.: Salt stress increases the level of translatable mRNA for phosphoenolpyruvate carboxylase in Mesembryanthemum crystallinum. - Plant Physiol. 84: 1270-1275, 1987. Go to original source...
    37. Semenov M., Blagodatskaya E., Stepanov A., Kuzyakov Y.: DNA-based determination of soil microbial biomass in alkaline and carbonaceous soils of semi-arid climate. - J. Arid Environ. 150: 54-61, 2018. Go to original source...
    38. Shen C., Yuan J., Qiao H. et al.: Transcriptomic and anatomic profiling reveal germination process of different wheat varieties in response to waterlogging stress. - BMC Genet. 21: 93, 2020. Go to original source...
    39. Shi B., Zhang J., Wang C. et al.: Responses of hydrolytic enzyme activities in saline-alkaline soil to mixed inorganic and organic nitrogen addition. - Sci. Rep.-UK 8: 4543, 2018. Go to original source...
    40. Singh R.K., Jaishankar J., Muthamilarasan M. et al.: Genome-wide analysis of heat shock proteins in C4 model, foxtail millet identifies potential candidates for crop improvement under abiotic stress. - Sci. Rep.-UK 6: 32641, 2016. Go to original source...
    41. South D.B.: Is the recommended pH for growing hardwood seedlings wrong? - Reforesta 7: 81-108, 2019. Go to original source...
    42. Sunagawa H., Cushman J., Agarie S.: Crassulacean acid metabolism may alleviate production of reactive oxygen species in a facultative CAM plant, the common ice plant Mesembryanthemum crystallinum L. - Plant Prod. Sci. 13: 256-260, 2010. Go to original source...
    43. Taticharoen T., Matsumoto S., Chutteang C. et al.: Response and acclimatization of a CAM orchid, Dendrobium Sonia 'Earsakul' to drought, heat, and combined drought and heat stress. - Sci. Hortic.-Amsterdam 309: 111661, 2023. Go to original source...
    44. Tsukagoshi H., Suzuki T., Nishikawa K. et al.: RNA-Seq analysis of the response of the halophyte, Mesembryanthemum crystallinum (ice plant) to high salinity. - PLoS ONE 10: e0118339, 2015. Go to original source...
    45. ul Haq S., Khan A., Ali M. et al.: Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. - Int. J. Mol. Sci. 20: 5321, 2019.
    46. Vivrette N.J., Muller C.H.: Mechanism of invasion and dominance of coastal grassland by Mesembryanthemum crystallinum. - Ecol. Monogr. 47: 301-318, 1977. Go to original source...
    47. Wakeel A., Gan Y.: A model for the ethylene-mediated auxin distribution under Cr (VI) stress in Arabidopsis thaliana. - Plant Signal. Behav. 13: e1473685, 2018. Go to original source...
    48. Wang Y., Ji H., Hu Y. et al.: Different selectivity in fungal communities between manure and mineral fertilizers: a study in an alkaline soil after 30 years fertilization. - Front. Microbiol. 9: 2613, 2018. Go to original source...
    49. Wang Z., Tan W., Yang D. et al.: Mitigation of soil salinization and alkalization by bacterium-induced inhibition of evaporation and salt crystallization. - Sci. Total Environ. 755: 142511, 2020. Go to original source...
    50. Wei L.-X., Lv B.-S., Wang M.-M. et al.: Priming effect of abscisic acid on alkaline stress tolerance in rice (Oryza sativa L.) seedlings. - Plant Physiol. Biochem. 90: 50-57, 2015. Go to original source...
    51. Wu B., Hou S., Peng D. et al.: Response of soil micro-ecology to different levels of cadmium in alkaline soil. - Ecotox. Environ. Safe. 166: 116-122, 2018. Go to original source...
    52. Yamamoto N., Sasou A., Saito Y. et al.: Protein and gene expression characteristics of a rice phosphoenolpyruvate carboxylase Osppc3; its unique role for seed cell maturation. - J. Cereal Sci. 64: 100-108, 2015. Go to original source...
    53. Yu S., Yu L., Hou Y. et al.: Contrasting effects of NaCl and NaHCO3 stresses on seed germination, seedling growth, photosynthesis, and osmoregulators of the common bean (Phaseolus vulgaris L.). - Agronomy 9: 409, 2019. Go to original source...
    54. Yu Y., Duan X., Ding X. et al.: A novel AP2/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis. - Plant Mol. Biol. 94: 509-530, 2017. Go to original source...
    55. Zhang C., Wu W., Xin X. et al.: Extract of ice plant (Mesembryanthemum crystallinum) ameliorates hyper­glycemia and modulates the gut microbiota composition in type 2 diabetic Goto-Kakizaki rats. - Food Funct. 10: 3252-3261, 2019. Go to original source...
    56. Zhang H., Liu X.-L., Zhang R.-X. et al.: Root damage under alkaline stress is associated with reactive oxygen species accumulation in rice (Oryza sativa L.). - Front. Plant Sci. 8: 1580, 2017. Go to original source...
    57. Zhang J., Wang P., Tian H. et al.: Identification of interior salt-tolerant bacteria from ice plant Mesembryanthemum crystallinum and evaluation of their promoting effects. - Symbiosis 76: 243-252, 2018. Go to original source...
    58. Zhang W.J., Niu Y., Bu S.H. et al.: Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage. - PLoS ONE 9: e84750, 2014. Go to original source...
    59. Zou C.-L., Wang Y.-B., Wang B. et al.: Effects of alkali stress on dry matter accumulation, root morphology, ion balance, free polyamines, and organic acids of sugar beet. - Acta Physiol. Plant. 43: 13, 2021. Go to original source...

    Return to the content