. State Key Laboratory of Efficient Utilization of Agricultural Water Resources, China Agricultural University, Beijing 100083, China . Center for Agricultural Water Research in China, China Agricultural University, Beijing 100083, China . National Field Scientific Observation and Research Station on Efficient Water Use of Oasis Agriculture in Wuwei of Gansu Province, Wuwei 733009, China . School of Nature Conservation, Beijing Forestry University, Beijing 100083, China
The investigation of the response mechanisms of Cyperus esculentus to water and salt stresses is crucial for the enhancement of the productivity of saline soils. Previous studies have indicated that plant hormones, antioxidant systems, and osmoregulation may contribute to the stabilization of yield. However, the contributions and interactions of these mechanisms remain poorly understood under combined water and salt stress in natural environments. A dual-factor (salt and water) orthogonal test was used to investigate the growth and biochemical responses of C. esculentus, under combined salt and water stress in a field experiment conducted on a typical saline area in northern China. The findings reveal that C. esculentus adjusted its biomass allocation strategies and activated hormone responses, antioxidant system, and osmoregulation mechanisms to maintain stable yield. Due to the negative synergism when salt and water stress coexist, the homogeneous limitations of both are weakened. Thus, the key to maintaining yields under combined water and salt stress may depend on indirectly enhancing tolerance to oxidative damage through abscisic acid, rather than focusing on accumulating low molecular weight osmoregulants and antioxidant enzymes to directly alleviate homogeneous limitations. Also, under combined salt and water stress, insufficient irrigation may have a greater impact on morphological characteristics than high salinity. The above results contribute to a deeper understanding of the process of adapting C. esculentus to combined salt and water stress.
Just Accepted Date: 29 August 2024Online First Date: 30 September 2024Issue Date: 12 November 2024
Cite this article:
Jing XU,Lang LIU,Fang KANG, et al. Abscisic acid-mediated yield gain through reduced oxidative damage caused by salt and water stress in Cyperus esculentus[J]. Front. Agr. Sci. Eng. ,
2024, 11(4): 561-574.
Fig.1 Experimental plot treatments and design. W0, control irrigation group; W1, moderate irrigation group; W2, low irrigation group; S0, control salinity group; S1, moderate salinity group; S2, heavy salinity group.
Fig.2 Response of measured variates in response to three levels each of salt and water treatment in field-grown in Cyperus esculentus. (a) LDW, leaf dry weight; (b) TDW, tuber dry weight; (c) RDW, root dry weight; (e) LA, leaf area; (d) R/S, ratio of root dry weight to leaf dry weight; (f) PH, plant height; (g) TLN, tiller number; and (h) TBN, tuber number. W0, control irrigation group; W1, moderate irrigation group; W2, low irrigation group; S0, control salinity group; S1, moderate salinity group; S2, heavy salinity group.
Fig.3 Concentration of nitrogen (a–c) and phosphorus (d–f) in the leaves, roots, and tubers under three levels each of salt and watering levels in field-grown in Cyperus esculentus. The significance (P < 0.05) between different treatment combinations is indicated above each column. W0, control irrigation group; W1, moderate irrigation group; W2, low irrigation group.
Fig.4 Active intracellular active substances in leaves of field-grown Cyperus esculentus under three levels each of salt and water treatment. DMT, dimethylthetin; SS, soluble sugars; Pro, proline; MDA, malonic dialdehyde; POD, peroxisome; SOD, superoxide dismutase; PEP, phosphoenolpyruvate; and ABA, abscisic acid. W0, control irrigation group; W1, moderate irrigation group; W2, low irrigation group; S0, control salinity group; S1, moderate salinity group; S2, heavy salinity group.
Fig.5 Structural equation modeling of associations between hormone response (abscisic acid), antioxidant regulation, osmoregulation, morphological characteristics and biomass in field-grown in Cyperus esculentus. The arrows in the diagram represent correlations between variables, with red arrows indicating positive correlations and blue arrows indicating negative correlations. Standardized path coefficients are shown in the middle of the arrows. The solid and dashed lines indicate the significance (P < 0.05) the correlations between variables. R2 represents the degree of explanation of potential variables in the model.
Fig.6 Principal component analysis clustering of morphological characteristics and biomass (a and b), and active intracellular substance (c and d) in field-grown in Cyperus esculentus under water (a and c) and salt (b and c) treatments. The treatments are represented by different colors for the individual points and 95% confidence ellipses. PC1, The first PCA components after downscaling; PC2, The second PCA components after downscaling. W0, control irrigation group; W1, moderate irrigation group; W2, low irrigation group; S0, control salinity group; S1, moderate salinity group; S2, heavy salinity group.
1
K, Ivushkin H, Bartholomeus A K, Bregt A, Pulatov B, Kempen Sousa L de . Global mapping of soil salinity change. Remote Sensing of Environment, 2019, 231: 111260 https://doi.org/10.1016/j.rse.2019.111260
2
S A, Shahid M, Zaman L Heng . Soil salinity: historical perspectives and a world overview of the problem. In: Zaman M, Shahid S A, Heng L, eds. Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques. Cham: Springer, 2018
3
P, Shrivastava R Kumar . Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences, 2015, 22(2): 123–131 https://doi.org/10.1016/j.sjbs.2014.12.001
4
X, Chang Z, Gao S, Wang H Chen . Modelling long-term soil salinity dynamics using SaltMod in Hetao Irrigation District, China. Computers and Electronics in Agriculture, 2019, 156: 447–458 https://doi.org/10.1016/j.compag.2018.12.005
5
D, Eswar R, Karuppusamy S Chellamuthu . Drivers of soil salinity and their correlation with climate change. Current Opinion in Environmental Sustainability, 2021, 50: 310–318 https://doi.org/10.1016/j.cosust.2020.10.015
6
A, Hassani A, Azapagic N Shokri . Global predictions of primary soil salinization under changing climate in the 21st century. Nature Communications, 2021, 12(1): 6663 https://doi.org/10.1038/s41467-021-26907-3
7
Z, Haj-Amor T, Araya D G, Kim S, Bouri J, Lee W, Ghiloufi Y, Yang H, Kang M K, Jhariya A, Banerjee R Lal . Soil salinity and its associated effects on soil microorganisms, greenhouse gas emissions, crop yield, biodiversity and desertification: a review. Science of the Total Environment, 2022, 843: 156946 https://doi.org/10.1016/j.scitotenv.2022.156946
8
M, Laxa M, Liebthal W, Telman K, Chibani K J Dietz . The role of the plant antioxidant system in drought tolerance. Antioxidants, 2019, 8(4): 94 https://doi.org/10.3390/antiox8040094
9
T, Yamaguchi E Blumwald . Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science, 2005, 10(12): 615–620 https://doi.org/10.1016/j.tplants.2005.10.002
10
Z Yang . Characteristics and Research Progress of Cyperus esculent. Northern Horticulture, 2017, (17): 192−201 (in Chinese)
11
R, Wang X, Wang H Xiang . A multipurpose emerging oil crop——Cyperus esculentus. China Oils Sand Fats, 2019, 44(1): 1−4 (in Chinese)
12
Y, Yu X, Lu T, Zhang C, Zhao S, Guan Y, Pu F Gao . Tiger nut (Cyperus esculentus L.): nutrition, processing, function and applications. Foods, 2022, 11(4): 601 https://doi.org/10.3390/foods11040601
13
N, Pascual-Seva B Pascual . Determination of crop coefficient for chufa crop (Cyperus esculentus L. var. sativus Boeck.) for sustainable irrigation scheduling. Science of the Total Environment, 2021, 768: 144975 https://doi.org/10.1016/j.scitotenv.2021.144975
14
X Zhang . Report on the research and development progress of China’s Cyperus esculentus L industry. China Rural Science & Technology, 2019, (4): 67−69 (in Chinese)
15
P Liang . Effect of mixed salinity stress on growth and ion absorption of Cyperus esculentus L. Thesis for the Master’s Degree. Shihezi, China: Shihezi University, 2022 (in Chinese)
16
R Tang . Response of seed germination and plant growth to saline alkali stress of Cyperus esculentus L. Thesis for the Master’s Degree. Shihezi, China: Shihezi University, 2022 (in Chinese)
17
A H, Dehghanipour B, Zahabiyoun G, Schoups H Babazadeh . A WEAP-MODFLOW surface water-groundwater model for the irrigated Miyandoab plain, Urmia lake basin, Iran: multi-objective calibration and quantification of historical drought impacts. Agricultural Water Management, 2019, 223: 105704 https://doi.org/10.1016/j.agwat.2019.105704
18
A, Litalien B Zeeb . Curing the earth: A review of anthropogenic soil salinization and plant-based strategies for sustainable mitigation. Science of the Total Environment, 2020, 698: 134235 https://doi.org/10.1016/j.scitotenv.2019.134235
V, Gunarathne M, Vithanage J Rinklebe . Overview of salinity in Arable soils: global perspectives. In: Bolan N, Kirkham M B, eds. Soil Constraints and Productivity. Boca Raton: CRC Press, 2023
21
L, Zhang M, Yu G, Ding C, Wang G, Gao F, Du W Mi . Effects of salt and alkali stress on the growth and physiological characteristics of Cyperus esculentus. Science of Soil and Water Conservation, 2022, 20(2): 65−71 (in Chinese)
22
Y, Wang G, Ding X, Cui M, Yu L Zhang . Effects of saline-alkali stress on the growth and photosynthetic characteristics of Cyperus esculentus and the responses of protective enzymes. Journal of Arid Land Resources and Environment, 2022, 36(5): 146−152 (in Chinese)
23
Z, Mu Z, Wei J, Liu Y, Cheng Y, Song H, Yao X, Yuan S, Wang Y, Gu J, Zhong K, Liu C, Li J, Du Q Zhang . RNA-Seq analysis demonstrates different strategies employed by tiger nuts (Cyperus esculentus L.) in response to drought stress. Life, 2022, 12(7): 1051 https://doi.org/10.3390/life12071051
24
B, Liu Y, Hu M, Li H, Xue Y, Wang Z Li . Effects of drought stress on the functional traits and rhizosphere microbial community structure of Cyperus esculentus. Grassland Science, 2024, 70(3): 109−120
25
J, Zhu L, Tian L, Xue X, Shi X Wang . Effects of different lrrigation volume on dry matter accumulation of Cyperus esculentus. Guizhou Agricultural Sciences, 2016, 44(4): 31–34+38 (in Chinese)
26
Y, Ding J, Yang L, Li Z, Zhang F Zeng . Effects of deficit irrigation and film mulching on biomass and production of Cyperus esculentus in the Southern Xiniiang Basin. Arid Zone Research, 2022, 39(3): 883−892 (in Chinese)
27
A, Abdelraheem N, Esmaeili M, O’Connell J Zhang . Progress and perspective on drought and salt stress tolerance in cotton. Industrial Crops and Products, 2019, 130: 118–129 https://doi.org/10.1016/j.indcrop.2018.12.070
28
S I, Zandalinas F B, Fritschi R Mittler . Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends in Plant Science, 2021, 26(6): 588–599 https://doi.org/10.1016/j.tplants.2021.02.011
29
R M, Rivero R, Mittler E, Blumwald S I Zandalinas . Developing climate‐resilient crops: improving plant tolerance to stress combination. Plant Journal, 2022, 109(2): 373–389 https://doi.org/10.1111/tpj.15483
30
I, Ahmed U, Nadira N, Bibi G, Zhang F Wu . Tolerance to combined stress of drought and salinity in barley. In: Mahalingam R, ed. Combined Stresses in Plants. Cham: Springer, 2015
31
P B, Angon M, Tahjib-Ul-Arif S I, Samin U, Habiba M A, Hossain M Brestic . How do plants respond to combined drought and salinity stress?—A systematic review. Plants, 2022, 11(21): 2884 https://doi.org/10.3390/plants11212884
32
C G, Kowalenko D Babuin . Interference problems with phosphoantimonylmolybdenum colorimetric measurement of phosphorus in soil and plant materials. Communications in Soil Science and Plant Analysis, 2007, 38(9−10): 1299–1316 https://doi.org/10.1080/00103620701328594
33
Y, Pokhrel F, Felfelani Y, Satoh J, Boulange P, Burek A, Gädeke D, Gerten S N, Gosling M, Grillakis L, Gudmundsson N, Hanasaki H, Kim A, Koutroulis J, Liu L, Papadimitriou J, Schewe Schmied H, Müller T, Stacke C E, Telteu W, Thiery T, Veldkamp F, Zhao Y Wada . Global terrestrial water storage and drought severity under climate change. Nature Climate Change, 2021, 11(3): 226–233 https://doi.org/10.1038/s41558-020-00972-w
34
L, Yang L, Lai J, Zhou Q, Li S, Yi Q, Sun Y Zheng . Changes in levels of enzymes and osmotic adjustment compounds in key species and their relevance to vegetation succession in abandoned croplands of a semiarid sandy region. Ecology and Evolution, 2020, 10(4): 2269–2280 https://doi.org/10.1002/ece3.6067
35
E, Ábrahám C, Hourton-Cabassa L, Erdei L Szabados . Methods for determination of proline in plants. In: Sunkar R, ed. Plant Stress Tolerance: Methods and Protocols. Cham: Springer, 2010
36
Y W, Zhang W W, Fan H, Li H, Ni H B, Han H H Li . Simultaneous column chromatographic extraction and purification of abscisic acid in peanut plants for direct HPLC analysis. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 2015, 1002: 277–284 https://doi.org/10.1016/j.jchromb.2015.08.033
37
Y Rosseel . lavaan: an R package for structural equation modeling. Journal of Statistical Software, 2012, 48(2): 1–36 https://doi.org/10.18637/jss.v048.i02
38
F E Jr, Harrell C Dupont . Hmisc: Harrell Miscellaneous. R package version 5.1–0. Available at CRAN website (CRAN.R-project.org/package=Hmis) on August 1, 2024
M F, Seleiman N, Al-Suhaibani N, Ali M, Akmal M, Alotaibi Y, Refay T, Dindaroglu H H, Abdul-Wajid M L Battaglia . Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants, 2021, 10(2): 259 https://doi.org/10.3390/plants10020259
41
V V, Kumari P, Banerjee V C, Verma S, Sukumaran M A S, Chandran K A, Gopinath G, Venkatesh S K, Yadav V K, Singh N K Awasthi . Plant nutrition: an effective way to alleviate abiotic stress in agricultural crops. International Journal of Molecular Sciences, 2022, 23(15): 8519 https://doi.org/10.3390/ijms23158519
42
J Y, Ye W H, Tian C W Jin . Nitrogen in plants: from nutrition to the modulation of abiotic stress adaptation. Stress Biology, 2022, 2(1): 4 https://doi.org/10.1007/s44154-021-00030-1
43
M, Nadeem J, Li M, Yahya A, Sher C, Ma X, Wang L Qiu . Research progress and perspective on drought stress in legumes: a review. International Journal of Molecular Sciences, 2019, 20(10): 2541 https://doi.org/10.3390/ijms20102541
44
Sabagh A, El A, Hossain C, Barutçular M A, Iqbal M S, Islam S, Fahad O, Sytar F, Çiğ R S, Meena M Erman . Consequences of salinity stress on the quality of crops and its mitigation strategies for sustainable crop production: an outlook of arid and semi-arid regions. In: Fahad S, Hasanuzzaman M, Alam M, Ullah H, Saeed M, Ali Khan I, Adnan M, eds. Environment, Climate, Plant and Vegetation Growth. Cham: Springer, 2020
45
A H, Naing C K Kim . Abiotic stress‐induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiologia Plantarum, 2021, 172(3): 1711–1723 https://doi.org/10.1111/ppl.13373
46
J, Alkahtani Y Dwiningsih . Analysis of morphological, physiological, and biochemical traits of salt stress tolerance in Asian Rice Cultivars at seedling and early vegetative stages. Stresses, 2023, 3(4): 717–735 https://doi.org/10.3390/stresses3040049
47
K K Nadarajah . ROS homeostasis in abiotic stress tolerance in plants. International Journal of Molecular Sciences, 2020, 21(15): 5208 https://doi.org/10.3390/ijms21155208
48
R, Mittler S I, Zandalinas Y, Fichman Breusegem F Van . Reactive oxygen species signalling in plant stress responses. Nature Reviews. Molecular Cell Biology, 2022, 23(10): 663–679 https://doi.org/10.1038/s41580-022-00499-2
49
B, Zhang L, Zhang M, Yu G, Ding G Gao . Evaluation of drought resistant ability and physiological mechanism in drought resistance of Cyperus esculentus var. sativus. Journal of Beijing Forestry University, 2022, 44(4): 107−115 (in Chinese)
50
M M, Chaves J, Flexas C Pinheiro . Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany, 2009, 103(4): 551–560 https://doi.org/10.1093/aob/mcn125
51
Oliveira A B, de Alencar N L, Mendes E Gomes-Filho . Comparison between the water and salt stress effects on plant growth and development. In: Akinci S, ed. Responses of Organisms to Water Stress. Rijeka: IntechOpen, 2013
52
Y, Ma M C, Dias H Freitas . Drought and salinity stress responses and microbe-induced tolerance in plants. Frontiers in Plant Science, 2020, 11: 591911 https://doi.org/10.3389/fpls.2020.591911
53
H, Cao R, Ding S, Kang T, Du L, Tong Y, Zhang J, Chen M K Shukla . Drought, salt, and combined stresses in plants: effects, tolerance mechanisms, and strategies. Advances in Agronomy, 2023, 178: 107–163 https://doi.org/10.1016/bs.agron.2022.11.004
54
W F Abobatta . Plant responses and tolerance to combined salt and drought stress. In: Hasanuzzaman M, Tanveer M, eds. Salt and Drought Stress Tolerance in Plants. Signaling Plant Responses and Tolerance to Combined Salt and Drought Stress. Cham: Springer, 2020
Z, Yu X, Duan L, Luo S, Dai Z, Ding G Xia . How plant hormones mediate salt stress responses. Trends in Plant Science, 2020, 25(11): 1117–1130 https://doi.org/10.1016/j.tplants.2020.06.008
57
S I, Zandalinas S, Sengupta F B, Fritschi R K, Azad R, Nechushtai R Mittler . The impact of multifactorial stress combination on plant growth and survival. New Phytologist, 2021, 230(3): 1034–1048 https://doi.org/10.1111/nph.17232
58
L, Shaar-Moshe E, Blumwald Z Peleg . Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat. Plant Physiology, 2017, 174(1): 421–434 https://doi.org/10.1104/pp.17.00030
59
S, Tiwari C, Lata P S, Chauhan V, Prasad M Prasad . A functional genomic perspective on drought signalling and its crosstalk with phytohormone-mediated signalling pathways in plants. Current Genomics, 2017, 18(6): 469–482 https://doi.org/10.2174/1389202918666170605083319
60
S I, Zandalinas Y, Fichman A R, Devireddy S, Sengupta R K, Azad R Mittler . Systemic signaling during abiotic stress combination in plants. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(24): 13810–13820 https://doi.org/10.1073/pnas.2005077117
61
S, Zhao Q, Zhang M, Liu H, Zhou C, Ma P Wang . Regulation of plant responses to salt stress. International Journal of Molecular Sciences, 2021, 22(9): 4609 https://doi.org/10.3390/ijms22094609
62
A, Wahab G, Abdi M H, Saleem B, Ali S, Ullah W, Shah S, Mumtaz G, Yasin C C, Muresan R A Marc . Plants’ physio-biochemical and phyto-hormonal responses to alleviate the adverse effects of drought stress: a comprehensive review. Plants, 2022, 11(13): 1620 https://doi.org/10.3390/plants11131620
63
T S, Per N A, Khan P S, Reddy A, Masood M, Hasanuzzaman M I R, Khan N A Anjum . Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiology and Biochemistry, 2017, 115: 126–140 https://doi.org/10.1016/j.plaphy.2017.03.018
64
A, Shomali S Aliniaeifard . Overview of signal transduction in plants under salt and drought stresses. In: Hasanuzzaman M, Tanveer M, eds. Salt and Drought Stress Tolerance in Plants. Signaling and Communication in Plants. Cham: Springer, 2020
65
M, He C Q, He N Z Ding . Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Frontiers in Plant Science, 2018, 9: 1771 https://doi.org/10.3389/fpls.2018.01771
66
H Torun . Time‐course analysis of salicylic acid effects on ROS regulation and antioxidant defense in roots of hulled and hulless barley under combined stress of drought, heat and salinity. Physiologia Plantarum, 2019, 165(2): 169–182 https://doi.org/10.1111/ppl.12798
67
L S, Pascual R, Mittler R, Sinha M Á, Peláez-Vico M F, López-Climent V, Vives-Peris A, Gómez-Cadenas S I Zandalinas . Jasmonic acid is required for tomato acclimation to multifactorial stress combination. Environmental and Experimental Botany, 2023, 213: 105425 https://doi.org/10.1016/j.envexpbot.2023.105425
68
S, Dayer J D, Scharwies S A, Ramesh W, Sullivan F C, Doerflinger V, Pagay S D Tyerman . Comparing hydraulics between two grapevine cultivars reveals differences in stomatal regulation under water stress and exogenous ABA applications. Frontiers in Plant Science, 2020, 11: 705 https://doi.org/10.3389/fpls.2020.00705
69
Q, Hussain M, Asim R, Zhang R, Khan S, Farooq J Wu . Transcription factors interact with ABA through gene expression and signaling pathways to mitigate drought and salinity stress. Biomolecules, 2021, 11(8): 1159 https://doi.org/10.3390/biom11081159
70
M M, Aslam M, Waseem B H, Jakada E J, Okal Z, Lei H S A, Saqib W, Yuan W, Xu Q Zhang . Mechanisms of abscisic acid-mediated drought stress responses in plants. International Journal of Molecular Sciences, 2022, 23(3): 1084 https://doi.org/10.3390/ijms23031084
71
N, Pascual-Seva Bautista A, San S, López-Galarza J V, Maroto B Pascual . Influence of different drip irrigation strategies on irrigation water use efficiency on chufa (Cyperus esculentus L. var. sativus Boeck.) crop. Agricultural Water Management, 2018, 208: 406–413 https://doi.org/10.1016/j.agwat.2018.07.003
