Foliar application of strigolactones improves the desiccation tolerance, grain yield and water use efficiency in dryland wheat through modulation of non-hydraulic root signals and antioxidant defense

Sha Guo, Xiaofei Wei, Baoluo Ma, Yongqing Ma, Zihan Yu, Pufang Li

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 54. DOI: 10.1007/s44154-023-00127-9
Original Paper

Foliar application of strigolactones improves the desiccation tolerance, grain yield and water use efficiency in dryland wheat through modulation of non-hydraulic root signals and antioxidant defense

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Abstract

Non-hydraulic root signals (nHRS) are affirmed as a unique positive response to soil drying, and play a crucial role in regulating water use efficiency and yield formation in dryland wheat production. Strigolactones (SLs) can enhance plant drought adaptability. However, the question of whether strigolactones enhance grain yield and water use efficiency by regulating nHRS and antioxidant defense systems in dryland wheat remains unanswered. In this study, pot experiments were conducted to investigate the effects of strigolactones on nHRS, antioxidant defense system, and grain yield and water use efficiency in dryland wheat. The results showed that external application of SLs increased drought-induced abscisic acid (ABA) accumulation and activated an earlier trigger of nHRS at 73.4% field capacity (FC), compared to 68.5% FC in the control group (CK). This phenomenon was mechanically associated with the physiological mediation of SLs. The application of SLs significantly enhanced the activities of leaf antioxidant enzymes, reduced ROS production, and mitigated oxidative damage to lipid membrane. Additionally, root biomass, root length density, and root to shoot ratio were increased under strigolactone treatment. Furthermore, exogenous application of SLs significantly increased grain yield by 34.9% under moderate drought stress. Water use efficiency was also increased by 21.5% and 33.3% under moderate and severe drought conditions respectively, compared to the control group (CK). The results suggested that the application of strigolactones triggered earlier drought-sensing mechanism and improved the antioxidant defense ability, thus enhancing grain yield and water use efficiency in dryland wheat production.

Keywords

Strigolactones / Non-hydraulic root signals / Antioxidant defense system / Grain yield / Water use efficiency

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Sha Guo, Xiaofei Wei, Baoluo Ma, Yongqing Ma, Zihan Yu, Pufang Li. Foliar application of strigolactones improves the desiccation tolerance, grain yield and water use efficiency in dryland wheat through modulation of non-hydraulic root signals and antioxidant defense. Stress Biology, 2023, 3(1): 54 https://doi.org/10.1007/s44154-023-00127-9

References

[1]
Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, London. pp 121–126.
[2]
Al-AmriAA, AlsubaieQD, AlamriSA, SiddiquiMH. Strigolactone analog GR24 induces seed germination and improves growth performance of different genotypes of tomato. J Plant Growth Regul, 2023, 42: 5653-5666
CrossRef Google scholar
[3]
AmakoK, ChenGX, AsadaK. Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol, 1994, 35: 497-504
CrossRef Google scholar
[4]
ArocaR, Ruiz-LozanoJM, ZamarreñoAM, PazJA, García-MinaJM, PozoMJ, López-RáezJA. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol, 2013, 170: 47-55
CrossRef Google scholar
[5]
AugéRM, DuanXG, CrokerJL, WitteWT, GreenCD. Foliar dehydration tolerance of 12 deciduous tree species. J Exp Bot, 1998, 49: 753-759
CrossRef Google scholar
[6]
BatoolA, AishaNA, ChengZG, LvGC, AshrafM, AfzalM, XiongJL, WangJY, XiongYC. Physiological and biochemical responses of two spring wheat genotypes to non-hydraulic root-to-shoot signaling of partial and full root-zone drought stress. Plant Physiol Bioch, 2019, 139: 11-20
CrossRef Google scholar
[7]
BollmarkM, KubátB, EliassonL. Variation in endogenous cytokinin content during adventitious root formation in pea cuttings. J Plant Physiol, 1988, 132: 262-265
CrossRef Google scholar
[8]
ChenQC, HuT, LiXH, SongCP, ZhuJK, ChenLQ, ZhaoY. Phosphorylation of SWEET sucrose transporters regulates plant root: shoot ratio under drought. Nat Plants, 2021, 8: 68-77
CrossRef Google scholar
[9]
DaviesWJ, ZhangJ. Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol Plant Mol Biol, 1991, 42: 55-76
CrossRef Google scholar
[10]
DongSM, DongYS, LiuB, LiuJ, LiuSK, ZhaoZY, LiWT, TianBS, ZhaoRX, HeF, GaiSL, XieY, YangPP, ZhaoYL. Guiding transition metal-doped hollow Cerium tandem nanozymes with elaborately regulated multi-enzymatic activities for intensive chemodynamic therapy. Adv Mater, 2022, 34: 2107054
CrossRef Google scholar
[11]
DuYL, WangZY, FanJW, TurnerNC, WangT, LiFM. β-Aminobutyric acid increases abscisic acid accumulation and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying. J Exp Bot, 2012, 63: 4849-4860
CrossRef Google scholar
[12]
EhdaieB, AlloushGA, WainesJG. Genotypic variation in linear rate of grain growth and contribution of stem reserves to grain yield in wheat. Field Crop Res, 2008, 106: 34-43
CrossRef Google scholar
[13]
EhdaieB, LayneAP, WainesJG. Root system plasticity to drought influences grain yield in bread wheat. Euphytica, 2012, 186: 219-232
CrossRef Google scholar
[14]
ElstnerEF, HeupelA. Inhibition of nitrite formation from hydroxylammoniumchloride: A simple assay for superoxide dismutase. Anal Biochem, 1976, 70: 616-620
CrossRef Google scholar
[15]
FanXW, LiFM, SongL, XiongYC, AnLZ, JiaY, FangXW. Defense strategy of old and modern spring wheat varieties during soil drying. Physiol Plantarum, 2009, 136: 310-323
CrossRef Google scholar
[16]
FangY, DuYL, WangJ, WuAJ, QiaoS, XuBC, ZhangSQ, SiddiqueKHM, ChenYL. Moderate drought stress affected root growth and grain yield in old, modern and newly released cultivars of winter wheat. Front Plant Sci, 2017, 8: 672
CrossRef Google scholar
[17]
GeY, CaiXM, ZhuTJ, RinglerC. Drought frequency change: an assessment in northern India plains. Agr Water Manage, 2016, 176: 111-121
CrossRef Google scholar
[18]
HimmelbauerML, LoiskandlW, KastanekF. Estimating length, average diameter and surface area of roots using two different Image analyses systems. Plant Soil, 2004, 260: 111-120
CrossRef Google scholar
[19]
JakabG, TonJ, FlorsV, ZimmerliL, MétrauxJP, Mauch-ManiB. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol, 2005, 139: 267-274
CrossRef Google scholar
[20]
JaleelCA, RiadhK, GopiR, ManivannanP, InesJ, Al-JuburiH, ZhaoCX, ShaoHB, PanneerselvamR. Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant, 2009, 31: 427-436
CrossRef Google scholar
[21]
LiR, ZhouXQ, LiuD, FengW. Enhancing the activity and stability of Mn-superoxide dismutase by one-by-one ligation to catalase. Free Radical Biol Med, 2018, 129: 138-145
CrossRef Google scholar
[22]
LiWQ, Herrera-EstrellaH, PhanLSP. Do cytokinins and strigolactones crosstalk during drought adaptation?. Trends Plant Sci, 2019, 24: 669-672
CrossRef Google scholar
[23]
LiBR, ZhangXY, MoritaS, SekiyaN, ArakiH, GuHJ, HanJ, LuY, LiuXW. Are crop deep roots always beneficial for combating drought: A review of root structure and function, regulation and phenotyping. Agric Water Manage, 2022, 271
CrossRef Google scholar
[24]
LiYB, WangYX, LiDX, WangF. Integrated drought evaluation index: considering the ecological feedback of the soil moisture and vegetation on wheat. Paddy Water Environ, 2022, 21: 127-150
CrossRef Google scholar
[25]
LiuFL, JensenCR, AndersenMN. Hydraulic and chemical signals in the control of leaf expansion and stomatal conductance in soybean exposed to drought stress. Funct Plant Biol, 2003, 30: 65-73
CrossRef Google scholar
[26]
LiuJW, HeHZ, VitaliM, VisentinI, CharnikhovaT, HaiderI, SchubertA, Ruyter-SpiraC, BouwmeesterHJ, LovisoloC, CardinaleF. Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta, 2015, 241: 1435-1451
CrossRef Google scholar
[27]
LiuX, HuQL, YanJJ, SunK, LiangY, JiaM, MengXB, FangS, WangYQ, JingYH, LiuGF, WuDX, ChuCC, SmithSM, ChuJF, WangYH, LiJY, WangB. ζ-Carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Mol Plant, 2020, 13: 1784-1801
CrossRef Google scholar
[28]
LvGC, ChengZG, LiFM, AkramNA, XiongYC. Comparative response to drought in primitive and modern wheat: a cue on domestication. Planta, 2019, 250: 629-642
CrossRef Google scholar
[29]
MaN, HuC, WanL, HuQ, XiongJL, ZhangCL. Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. Front Plant Sci, 2017, 8: 1671
CrossRef Google scholar
[30]
MatthysC, WaltonA, StrukS, StesE, BoyerFD, GevaertK, GoormachtigS. The whats, the wheres and the hows of strigolactone action in the roots. Planta, 2016, 243: 1327-1337
CrossRef Google scholar
[31]
MinZ, LiRY, ChenL, ZhangY, LiZY, LiuM, JuYL, FangYL. Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiol Biochem, 2019, 135: 99-110
CrossRef Google scholar
[32]
RazaA, SalehiH, RahmanMA, ZahidZ, HaghjouMM, Najafi-KakavandS, CharaghS, OsmanHS, AlbaqamiM, ZhuangYH, SiddiqueKHM, ZhuangWJ. Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Front Plant Sci, 2022, 13
CrossRef Google scholar
[33]
ReynoldsM, DreccerF, TrethowanR. Drought-adaptive traits derived from wheat wild relatives and landraces. J Exp Bot, 2007, 52: 177-186
CrossRef Google scholar
[34]
Ruiz-LozanoJM, ArocaR, ZamarreñoAM, MolinaS, Andreo-JiménezB, PorcelR, García-MinaJM, Ruyter-SpiraC, López-RáezJA. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ, 2015, 39: 441-452
CrossRef Google scholar
[35]
RuszkowskiM, NocekB, ForlaniG, DauterZ. The structure of Medicago truncatula delta (1)-pyrroline-5-carboxylate reductase provides new insights into regulation of proline biosynthesis in plants. Front Plant Sci, 2015, 6: 869
CrossRef Google scholar
[36]
SchaedleM, BasshamJA. Chloroplast glutathione reductase. Plant Physiol, 1977, 59: 1011-1012
CrossRef Google scholar
[37]
SedaghatM, EmamY, Mokhtassi-BidgoliA, HazratiS, LovisoloC, VisentinI, CardinaleF, Tahmasebi-SarvestaniZ. The potential of the synthetic strigolactone analogue GR24 for the maintenance of photosynthesis and yield in winter wheat under drought: investigations on the mechanisms of action and delivery modes. Plants-Basel, 2021, 10: 1223
CrossRef Google scholar
[38]
SeleimanMF, Al-SuhaibaniN, AliN, AkmalM, AlotaibiM, RefayY, DindarogluT, Abdul-WajidHH, BattagliaML. Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants-Basel, 2021, 10: 259
CrossRef Google scholar
[39]
SunHW, LiWQ, BurrittDJ, TianHT, ZhangH, LiangXH, MiaoYC, MostofaMG, TranLSP. Strigolactones interact with other phytohormones to modulate plant root growth and development. Crop J, 2022, 10: 1517-1527
CrossRef Google scholar
[40]
TomJD, LesperanceML. Piecewise regression: a tool for identifying ecological thresholds. Ecology, 2003, 84: 2034-2041
CrossRef Google scholar
[41]
TurnerNC. Further progress in crop water relations. Adv Agron, 1996, 58: 293-338
CrossRef Google scholar
[42]
TurnerNC, BlumA, CakirM, StedutoP, TuberosaR, YoungN. Strategies to increase the yield and yield stability of crops under drought - are we making progress?. Funct Plant Biol, 2014, 41: 1199-1206
CrossRef Google scholar
[43]
UpadhyayaH, DuttaBK, PandaSK. Zinc Modulates drought-induced biochemical damages in tea [Camellia sinensis (L) O Kuntze]. J Agric Food Chem, 2013, 61: 6660-6670
CrossRef Google scholar
[44]
VisentinI, PagliaraniC, DevaE, CaracciA, TureckovaV, NovakO, LovisoloC, SchubertA, CardinaleF. A novel strigolactone-miR156 module controls stomatal behavior during drought recovery. Plant Cell Physiol, 2020, 43: 1613-1624
CrossRef Google scholar
[45]
WangYQ, GaoFL, GaoGY, ZhaoJY, WangXG, ZhangR. Production and cultivated area variation in cereal, rice, wheat and maize in China (1998–2016). Agronomy, 2019, 9: 222
CrossRef Google scholar
[46]
WangJY, LiCN, LiL, ReynoldsM, MaoXG, JingRL. Exploitation of drought tolerance-related genes for crop improvement. Int J Mol Sci, 2021, 22: 10265
CrossRef Google scholar
[47]
WangYJ, FangBT, DuSM, LiXD. The effect of wheat drought resistance by different concentrations exogenous strigolactone. J Biobased Mater Bioenergy, 2022, 16: 653-658
CrossRef Google scholar
[48]
XiaoJ, LiuB, YaoYY, GuoZF, JiaHY, KongLR, ZhangAM, MaWJ, NiZF, XuSB, LuF, JiaoYN, YangWY, LinXL, SunSL, LuZF, GaoLF, ZhaoGY, CaoSH, ChenQ, ZhangKP, WangMC, WangM, HuZR, GuoWL, LiGQ, MaX, LiJM, HanFP, FuXD, MaZQ, WangDW, ZhangXY, LingHQ, XiaGM, TongYP, LiuZY, HeZH, JiaJZ, ChongK. Wheat genomic study for genetic improvement of traits in China. Sci China Life Sci, 2022, 65: 1718-1775
CrossRef Google scholar
[49]
XiongYC, LiFM, ZhangT. Performance of wheat crops with different chromosome ploidy: root-sourced signals, drought tolerance, and yield performance. Planta, 2006, 224: 710-718
CrossRef Google scholar
[50]
XiongYC, LiFM, XuBC, HodgkinsonKC. Hydraulic and non-hydraulic root-sourced signals in old and modern spring wheat cultivars in a semiarid area. J Plant Growth Regul, 2006, 25: 120-136
CrossRef Google scholar
[51]
XuJH, LiLJ, LiuYF, YuYY, LiH, WangX, PangYN, CaoH, SunQH. Molecular and physiological mechanisms of strigolactones-mediated drought stress in crab apple (Malus hupehensis Rehd.) seedlings. Sci Hortic- amsterdam, 2023, 311: 111800
CrossRef Google scholar
[52]
YangJC, ZhangJH, WangZQ, ZhuQS, WangW. Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol, 2001, 127: 315-323
CrossRef Google scholar
[53]
YangYW, GuMZ, LuJF, LiXT, LiuDL, LiXE, WangL. GR24 alleviates the adverse effects of drought stress on physiology and photosystem II function in alfalfa (Medicago sativa L.). Grassl Sci, 2023, 69: 113-119
CrossRef Google scholar
[54]
YinY, WangGZ, LiuYK, WangXF, GaoWS, ZhangS, YouCX. Simple phenotypic sensor for visibly tracking H2O2 fluctuation to detect plant health status. J Agric Food Chem, 2022, 70: 10058-10064
CrossRef Google scholar
[55]
ZhangFP, SussmilchF, NicholsDS, CardosoAA, BrodribbTJ, McAdamSAM. Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. J EXP BOT, 2018, 69: 1261-1267
CrossRef Google scholar
[56]
ZhangYH, XiaoYZ, ZhangYA, DongY, LiuYQ, LiuL, WanSQ, HeJY, YuYB. Accumulation of galactinol and ABA is involved in exogenous EBR-induced drought tolerance in tea plants. J Agric Food Chem, 2022, 70: 13391-13403
CrossRef Google scholar
[57]
ZhaoBQ, LiuQY, WangBS, YuanF. Roles of phytohormones and their signaling pathways in leaf development and stress responses. J Agric Food Chem, 2021, 69: 3566-3584
CrossRef Google scholar
Funding
the National Natural Science Foundation of China(31901123)

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