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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Specific physiological responses to alkaline carbonate stress in rice (Oryza sativa) seedlings: organic acid metabolism and hormone signalling

Dan Wang A B # , Miao Xu B # , Teng-yuan Xu A , Xiu-yun Lin C , Elshan Musazade B , Jing-mei Lu D , Wei-jie Yue A , Li-quan Guo https://orcid.org/0000-0003-3424-2238 B * and Yu Zhang E *
+ Author Affiliations
- Author Affiliations

A School of Public Health, Jilin Medical University, Jilin 132013, PR China.

B College of Life Sciences, Jilin Agricultural University, Changchun 130118, PR China.

C Jilin Academy of Agricultural Sciences, Changchun 130118, PR China.

D School of Life Sciences, Jilin University, Changchun 130062, PR China.

E Land Requisition Affairs Center of Jilin Province, Changchun 130061, PR China.


Handling Editor: Fanrong Zeng

Functional Plant Biology 51, FP23161 https://doi.org/10.1071/FP23161
Submitted: 28 July 2023  Accepted: 28 August 2024  Published: 19 September 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

In recent years, alkaline soda soil has stimulated numerous biological research on plants under carbonate stress. Here, we explored the difference in physiological regulation of rice seedlings between saline (NaCl) and alkaline carbonate (NaHCO3 and Na2CO3) stress. The rice seedlings were treated with 40 mM NaCl, 40 mM NaHCO3 and 20 mM Na2CO3 for 2 h, 12 h, 24 h and 36 h, their physiological characteristics were determined, and organic acid biosynthesis and metabolism and hormone signalling were identified by transcriptome analysis. The results showed that alkaline stress caused greater damage to their photosynthetic and antioxidant systems and led to greater accumulation of organic acid, membrane damage, proline and soluble sugar but a decreased jasmonic acid content compared with NaCl stress. Jasmonate ZIM-Domain (JAZ), the probable indole-3-acetic acid-amido synthetase GH3s, and the protein phosphatase type 2Cs that related to the hormone signalling pathway especially changed under Na2CO3 stress. Further, the organic acid biosynthesis and metabolism process in rice seedlings were modified by both Na2CO3 and NaHCO3 stresses through the glycolate/glyoxylate and pyruvate metabolism pathways. Collectively, this study provides valuable evidence on carbonate-responsive genes and insights into the different molecular mechanisms of saline and alkaline stresses.

Keywords: abscisic acid (ABA) signalling, alkaline stress, auxin signalling, jasmonic acid (JA) signalling, organic acid biosynthesis, rice, transcriptome analysis, UDP-glycosyltransferase.

References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121-126.
| Crossref | Google Scholar | PubMed |

Ali MS, Baek KH (2020) Jasmonic acid signaling pathway in response to abiotic stresses in plants. International Journal of Molecular Sciences 21, 621-628.
| Crossref | Google Scholar | PubMed |

An XH, Hao YJ, Li EM, Xu K, Cheng CG (2017) Functional identification of apple MdJAZ2 in Arabidopsis with reduced JA-sensitivity and increased stress tolerance. Plant Cell Reports 36, 255-265.
| Crossref | Google Scholar | PubMed |

Blakeslee JJ, Spatola Rossi T, Kriechbaumer V (2019) Auxin biosynthesis: spatial regulation and adaptation to stress. Journal of Experimental Botany 70, 5041-5049.
| Crossref | Google Scholar | PubMed |

Chen W, Cui P, Sun H, Guo W, Yang C, Jin H, Fang B, Shi D (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.). Industrial Crops and Products 30, 351-358.
| Crossref | Google Scholar |

Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
| Crossref | Google Scholar | PubMed |

Food and Agriculture Organization of the United Nations (2021) World map of salt-affected soils launched at virtual conference. Available at https://www.fao.org/newsroom/detail/salt-affected-soils-map-symposium/en

Franceschi VR, Nakata PA (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41-71.
| Crossref | Google Scholar | PubMed |

Gao JS, Cai YP (2018) ‘Experimental guidance in plant physiology.’ (China Agricultural University Press: Beijing, China)

Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309-314.
| Crossref | Google Scholar | PubMed |

Gong B, Wen D, Bloszies S, Li X, Wei M, Yang F, Shi Q, Wang X (2014) Comparative effects of NaCl and NaHCO3 stresses on respiratory metabolism, antioxidant system, nutritional status, and organic acid metabolism in tomato roots. Acta Physiologiae Plantarum 36, 2167-2181.
| Crossref | Google Scholar |

Guo LQ, Shi DC, Wang DL (2010) The key physiological response to alkali stress by the alkali-resistant halophyte Puccinellia tenuiflora is the accumulation of large quantities of organic acids and into the rhyzosphere. Journal of Agronomy and Crop Science 196, 123-135.
| Crossref | Google Scholar |

Hu L, Zhang P, Jiang Y, Fu J (2015) Metabolomic analysis revealed differential adaptation to salinity and alkalinity stress in Kentucky Bluegrass (Poa pratensis L). Plant Molecular Biology Reporter 33, 56-68.
| Crossref | Google Scholar |

Hu Y, Huang Y, Zhou S, Zhang Y, Cheng R, Guo J, Ling Y (2020) Traditional rice landraces in Lei-Qiong area of South China tolerate salt stress with strong antioxidant activity. Plant Signaling & Behavior 15, 1740466.
| Crossref | Google Scholar | PubMed |

Huang XX, Zhao SM, Zhang YY, Li YJ, Shen HN, Li X, Hou BK (2021) A novel UDP-glycosyltransferase 91C1 confers specific herbicide resistance through detoxification reaction in Arabidopsis. Plant Physiology and Biochemistry 159, 226-233.
| Crossref | Google Scholar | PubMed |

Kaur R, Zhawar VK (2021) Regulation of secondary antioxidants and carbohydrates by gamma-aminobutyric acid under salinity–alkalinity stress in rice (Oryza sativa L.). Biologia Futura 72, 229-239.
| Crossref | Google Scholar | PubMed |

Kawanabe S, Zhu TC (1991) Degeneration and conservational trial of Aneurolepidium chinense grassland in northern China. Japanese Journal of Grassland Science 37, 91-99.
| Google Scholar |

Klapheck S, Zimmer I, Cosse H (1990) Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant and Cell Physiol 31, 1005-1013.
| Crossref | Google Scholar |

Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359.
| Crossref | Google Scholar | PubMed |

Leyser O (2017) Auxin signaling. Plant Physiology 176, 465-479.
| Crossref | Google Scholar | PubMed |

Li H, Chen H, Deng S, Cai H, Shi L, Xu F, Wang C (2021a) Inhibition of nitric oxide production under alkaline conditions regulates iron homeostasis in rice. Physiologia Plantarum 172, 1465-1476.
| Crossref | Google Scholar | PubMed |

Li Q, Qiao X, Jia L, Zhang Y, Zhang S (2021b) Transcriptome and resequencing analyses provide insight into differences in organic acid accumulation in two pear varieties. International Journal of Molecular Sciences 22, 9622.
| Crossref | Google Scholar |

Li H, Xu C, Han L, Li C, Xiao B, Wang H, Yang C (2022) Extensive secretion of phenolic acids and fatty acids facilitates rhizosphere pH regulation in halophyte Puccinellia tenuiflora under alkali stress. Physiologia Plantarum 174, e13678.
| Crossref | Google Scholar | PubMed |

Lunde C, Drew DP, Jacobs AK, Tester M (2007) Exclusion of Na+ via sodium ATPase (PpENA1) ensures normal growth of Physcomitrella patens under moderate salt stress. Plant Physiology 144, 1786-1796.
| Crossref | Google Scholar | PubMed |

Ma Q, Wu C, Liang S, Yuan Y, Liu C, Liu J, Feng B (2021) The alkali tolerance of broomcorn millet (Panicum miliaceum L.) at the germination and seedling stage: the case of 296 broomcorn millet genotypes. Frontiers in Plant Science 12, 711429.
| Crossref | Google Scholar | PubMed |

Malekzadeh P (2015) Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.). Physiology and Molecular Biology of Plants 21, 225-232.
| Crossref | Google Scholar | PubMed |

Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet Journal 17, 10-12.
| Crossref | Google Scholar |

Meech R, Hu DG, McKinnon RA, Mubarokah SN, Haines AZ, Nair PC, Rowland A, Mackenzie PI (2019) The UDP-Glycosyltransferase (UGT) superfamily: new members, new functions, and novel paradigms. Physiological Reviews 99, 1153-1222.
| Crossref | Google Scholar | PubMed |

Mellidou I, Koukounaras A, Kostas S, Patelou E, Kanellis AK (2021) Regulation of vitamin C accumulation for improved tomato fruit quality and alleviation of abiotic stress. Genes 12, 694-718.
| Crossref | Google Scholar | PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651-681.
| Crossref | Google Scholar | PubMed |

Nampei M, Jiadkong K, Chuamnakthong S, Wangsawang T, Sreewongchai T, Ueda A (2021) Different rhizospheric pH conditions affect nutrient accumulations in rice under salinity stress. Plants 10, 1295.
| Crossref | Google Scholar |

Peethambaran PK, Glenz R, Höninger S, Shahinul Islam SM, Hummel S, Harter K, Kolukisaoglu Ü, Meynard D, Guiderdoni E, Nick P, Riemann M (2018) Salt-inducible expression of OsJAZ8 improves resilience against salt-stress. BMC Plant Biology 18, 311.
| Crossref | Google Scholar | PubMed |

Quint M, Gray WM (2006) Auxin signaling. Current Opinion in Plant Biology 9, 448-453.
| Crossref | Google Scholar | PubMed |

Rehman HM, Nawaz MA, Shah ZH, Ludwig-Müller J, Chung G, Ahmad MQ, Yang SH, Lee SI (2018) Comparative genomic and transcriptomic analyses of Family-1 UDP glycosyltransferase in three Brassica species and Arabidopsis indicates stress-responsive regulation. Scientific Reports 8, 1875-1882.
| Crossref | Google Scholar | PubMed |

Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic acid signaling pathway in plants. International Journal of Molecular Sciences 20, 2479.
| Crossref | Google Scholar |

Shi H, Wang Y, Cheng Z, Ye T, Chan Z (2012) Analysis of natural variation in bermudagrass (Cynodon dactylon) reveals physiological responses underlying drought tolerance. PLoS ONE 7, e53422.
| Crossref | Google Scholar | PubMed |

Sirén J, Välimäki N, Mäkinen V (2014) Indexing graphs for path queries with applications in genome research. IEEE/ACM Transactions on Computational Biology and Bioinformatics 11, 375-388.
| Crossref | Google Scholar | PubMed |

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503-527.
| Crossref | Google Scholar | PubMed |

Tin HQ, Loi NH, Labarosa SJE, McNally KL, McCouch S, Kilian B (2021) Phenotypic response of farmer-selected CWR-derived rice lines to salt stress in the Mekong Delta. Crop Science 61, 201-218.
| Crossref | Google Scholar |

Valenzuela CE, Acevedo-Acevedo O, Miranda GS, Vergara-Barros P, Holuigue L, Figueroa CR, Figueroa PM (2016) Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. Journal of Experimental Botany 67, 4209-4220.
| Crossref | Google Scholar | PubMed |

Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biology 16, 86-92.
| Crossref | Google Scholar | PubMed |

Wang F, Guo Z, Li H, Wang M, Onac E, Zhou J, Xia X, Shi K, Yu J, Zhou Y (2016) Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiology 170, 459-471.
| Crossref | Google Scholar | PubMed |

Wei LX, Lv BS, Wang MM, Ma HY, Yang HY, Liu XL, Jiang CJ, Liang ZW (2015) Priming effect of abscisic acid on alkaline stress tolerance in rice (Oryza sativa L.) seedlings. Plant Physiology and Biochemistry 90, 50-57.
| Crossref | Google Scholar | PubMed |

Wu H, Ye H, Yao R, Zhang T, Xiong L (2015) OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Science 232, 1-12.
| Crossref | Google Scholar | PubMed |

Xiang G, Ma W, Gao S, Jin Z, Yue Q, Yao Y (2019) Transcriptomic and phosphoproteomic profiling and metabolite analyses reveal the mechanism of NaHCO3-induced organic acid secretion in grapevine roots. BMC Plant Biology 19, 383.
| Crossref | Google Scholar | PubMed |

Yan J, Li H, Li S, Yao R, Deng H, Xie Q, Xie D (2013) The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. The Plant Cell 25, 486-498.
| Crossref | Google Scholar | PubMed |

Yu L, Jiang J, Zhang C, Jiang L, Ye N, Lu Y, Yang G, Liu E, Peng C, He Z, Peng X (2010) Glyoxylate rather than ascorbate is an efficient precursor for oxalate biosynthesis in rice. Journal of Experimental Botany 61, 1625-1634.
| Crossref | Google Scholar | PubMed |

Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends in Plant Science 25, 1117-1130.
| Crossref | Google Scholar | PubMed |

Zhang H, Liu XL, Zhang RX, Yuan HY, Wang MM, Yang HY, Ma HY, Liu D, Jiang CJ, Liang ZW (2017) Root damage under alkaline stress is associated with reactive oxygen species accumulation in rice (Oryza sativa L.). Frontiers in Plant Science 8, 1580.
| Crossref | Google Scholar | PubMed |

Zhang Y, Fang J, Wu X, Dong L (2018) Na+/K+ balance and transport regulatory mechanisms in weedy and cultivated rice (Oryza sativa L.) under salt stress. BMC Plant Biology 18, 375.
| Crossref | Google Scholar | PubMed |

Zhang K, Sun Y, Li M, Long R (2021) CrUGT87A1, a UDP-sugar glycosyltransferases (UGTs) gene from Carex rigescens, increases salt tolerance by accumulating flavonoids for antioxidation in Arabidopsis thaliana. Plant Physiology and Biochemistry 159, 28-36.
| Crossref | Google Scholar | PubMed |

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66-71.
| Crossref | Google Scholar | PubMed |

Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167, 313-324.
| Crossref | Google Scholar | PubMed |