Humic Substances Involved in Plant Abiotic Stress Response: A Review on the Mechanism

doi:10.11924/j.issn.1000-6850.casb2022-0324

Abstract

Abstract:

In order to study the mechanism of humic substances (HS), a natural isomeric polymer organic compound, participating in plant abiotic stress response, this study summarized the following main mechanisms, including the HS mediated regulation of (PM) H⁺-ATPase, the HS mediated interaction of cell signal molecules, the shielding of HS adsorption layer, the chelation of HS chemical functional groups, and the impacts of HS on plant secondary metabolism and rhizosphere microbial community. It is concluded that HS participates in the regulation of abiotic stress response through a variety of complex defense metabolic mechanisms. Given the complexity of HS biochemistry, as well as many problems in the research of physiological activity and defense metabolism mechanism, future scientific research should mainly focus on the analysis of chemical composition and molecular structure of HS, how HS “colloidal stress” participates in metabolic regulation, the cross interference and feedback regulation mechanism of HS promoting and defense metabolism pathways, and the interaction mechanism between HS and soil microorganisms.

Key words: humic substances, abiotic stress, H⁺-ATPase, signal molecules, adsorption layer, functional groups, plant secondary metabolism, rhizosphere microbial community

SONG Ge, SHI Feng. Humic Substances Involved in Plant Abiotic Stress Response: A Review on the Mechanism[J]. Chinese Agricultural Science Bulletin, 2023, 39(15): 59-68.

Figures/Tables 3

References 93

[1]	CANELLSA L P, OLIVARES F L, AGUIAR N O, et al. Humic and fulvic acids as biostimulants in horticulture[J]. Scientia horticulturae, 2015, 196:15-27. doi: 10.1016/j.scienta.2015.09.013 URL
[2]	STEVENSON F J. Humus chemistry: genesis, composition, reaction[M]. 2nd ed. New York: Wiley and Sons, 1994.
[3]	DOU S, SHAN J, SONG X, et al. Are humic substances soil microbial residues or unique synthesized compounds? a perspective on their distinctiveness[J]. Pedosphere, 2020, 30(2):159-167. doi: 10.1016/S1002-0160(20)60001-7 URL
[4]	NEBBIOSO A, PICCOLO A. Advances in humeomics: enhanced structural identification of humic molecules after size fractionation of a soil humic acid[J]. Analytica chimica acta, 2012, 720:77-79. doi: 10.1016/j.aca.2012.01.027 pmid: 22365124
[5]	MELO DE B A G, MOTTA F L, SANTANA M H, et al. Humic acids: structural properties and multiple functionalities for novel technological developments[J]. Materials science and engineering C, 2016, 62:967-974. doi: 10.1016/j.msec.2015.12.001 URL
[6]	KALYONCU O, AKINCI S, BOZKURT E. The effects of humic acid on growth and ion uptake of mung bean (Vigna radiata (L. ) Wilczek) grown under salt stress[J]. African journal of agricultural research, 2017, 12(49): 3447-3460. doi: 10.5897/AJAR URL
[7]	MOSA A, TAHA A A, ELSAEID M. Agro-environmental applications of humic substances: a critical review[J]. Egyptian journal of soil science, 2020, 60(3):211-229.
[8]	JINDO K, CANELLAS L P, ALBACETE A, et al. Interaction between humic substances and plant hormones for phosphorous acquisition[J]. Agronomy, 2020, 10(5):640. doi: 10.3390/agronomy10050640 URL
[9]	HOHM T, DEMARSY E, QUAN C, et al. Plasma membrane H⁺-ATPase regulation is required for auxin gradient formation preceding phototropic growth[J]. Molecular systems biology, 2014, 10:751. doi: 10.15252/msb.20145247 URL
[10]	WANG P, YU W, ZHANG J, et al. Auxin enhances aluminum-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H⁺-ATPase in soybean roots[J]. Annals of botany, 2016, 118:933-940. doi: 10.1093/aob/mcw133 URL
[11]	ZHANG J, WEI J, LI D, et al. The role of the plasma membrane H⁺-ATPase in plant responses to aluminum toxicity[J]. Frontiers in plant science, 2017, 8:1757. doi: 10.3389/fpls.2017.01757 URL
[12]	BHATT D, SHARMA G. Role of silicon in counteracting abiotic and biotic plant stresses[J]. International journal of chemical studies, 2018, 6(2):1434-1442.
[13]	AYDIN A, KANT C, TURAN M, et al. Humic acid application alleviates salinity stress of bean (Phaseolus vulgaris L.) plants decreasing membrane leakage[J]. African journal of agricultural research, 2012, 7:1073-1086.
[14]	LOTFI R, GHARAVI -KOUCHEBAGH P, KHOSHVAGHTI H. Biochemical and physiological responses of Brassica napus plants to humic acid under water stress[J]. Russian journal of plant physiology, 2015, 62:480-486. doi: 10.1134/S1021443715040123 URL
[15]	MOGHADAM H R T. Humic acid as an ecological pathway to protect corn plants against oxidative stress[J]. Biological forum, 2015, 7(1):1704-1709.
[16]	ZANDONADI D B, SANTOS M P, DOBBSS L B, et al. Nitric oxide mediates humic acids-induced root development and plasma membrane H⁺-ATPase activation[J]. Planta, 2010, 231:1025-1036. doi: 10.1007/s00425-010-1106-0 pmid: 20145950
[17]	FRESCHI L. Nitric oxide and phytohormone interactions: current status and perspectives[J]. Frontiers in plant science, 2013, 4:398. doi: 10.3389/fpls.2013.00398 pmid: 24130567
[18]	HUANG A X, SHEB X P, ZHANG Y Y, et al. Cytosolic acidifi cation precedes nitric oxide removal during inhibition of ABA induced stomatal closure by fusicoccin[J]. Russian journal of plant physiology, 2013, 60:60-68. doi: 10.1134/S1021443712060076 URL
[19]	HANCOCK J T, NEILL S J, WILSON I D. Nitric oxide and ABA in the control of plant function[J]. Plant science, 2011, 181:555-559. doi: 10.1016/j.plantsci.2011.03.017 pmid: 21893252
[20]	MORA V, BACAICOA E, BAIGORRI R, et al. NO and IAA key regulators in the shoot growth promoting action of humic acid in Cucumis sativus L.[J]. Journal of plant growth regulation, 2014, 33:430-439. doi: 10.1007/s00344-013-9394-9 URL
[21]	SIDDIQUI M H, AL-WHAIBI M H, BASALAH M O. Role of nitric oxide in tolerance of plants to abiotic stress[J]. Protoplasma, 2011, 248:447-455. doi: 10.1007/s00709-010-0206-9 pmid: 20827494
[22]	DEMIDCHIK V, SHABALA SN, DAVIES JM, et al. Spatial variation in H₂O₂ response of Arabidopsis thaliana root epidermal Ca²⁺ flux and plasma membrane Ca²⁺ channels[J]. The plant journal, 2007, 49(3):377-386. doi: 10.1111/tpj.2007.49.issue-3 URL
[23]	RAMOS A C, DOBBSS L B, SANTOS L A, et al. Humic matter elicits proton and calcium fluxes and signaling dependent on Ca²⁺-dependent protein kinase (CDPK) at early stages of lateral plant root development[J]. Chemical and biological technologies in agriculture, 2015, 2:3. doi: 10.1186/s40538-014-0030-0 URL
[24]	OLAETXEA M, HITA D D, GARCIA A, et al. Hypothetical framework integrating the main mechanisms involved in the promoting action of rhizospheric humic substances on plant root- and shoot-growth[J]. Applied soil ecology, 2018, 123:521-537. doi: 10.1016/j.apsoil.2017.06.007 URL
[25]	CORDEIRO F C, SANTA-CATARINA C, SILVEIRA V, et al. ROS signaling: the new wave?[J]. Trends in plant science, 2011b, 16:300-309. doi: 10.1016/j.tplants.2011.03.007 URL
[26]	KULIKOVA N, PERMINOVA I, BADUN G, et al. Estimation of uptake of humic substances from different sources by Escherichia coli cells under optimum and salt stress conditions by use of tritium-labeled humic materials[J]. Applied and environmential microbiology, 2010, 76(18):6223-6230.
[27]	ASLI S, NEUMANN P M. Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development[J]. Plant and soil, 2010, 336:313-322. doi: 10.1007/s11104-010-0483-2 URL
[28]	HOSE E, STEUDLE E, HARTUNG W. Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes[J]. Planta, 2000, 211:874-882. pmid: 11144273
[29]	KULIKOVA N A, ABROSKIN D P, BADUN G A, et al. Label distribution in tissues of wheat seedlings cultivated with tritium-labeled leonardite humic acid[J]. Scientific reports, 2016, 6:28869. doi: 10.1038/srep28869 pmid: 27350412
[30]	OLAETXEA M, MORA V, BACAICOA E, et al. Abscisic acid regulation of root hydraulic conductivity and aquaporin gene expression is crucial to the plant shoot growth enhancement caused by rhizosphere humic acids[J]. Plant physiology, 2015, 169:2587-2596. doi: 10.1104/pp.15.00596 pmid: 26450705
[31]	ERTURK F A, AGAR G, ARSLAN E, et al. Analysis of genetic and epigenetic effects of maize seeds in response to heavy metal (Zn)stress[J]. Environmental science and pollution research, 2015, 22:10291-10297. doi: 10.1007/s11356-014-3886-4 URL
[32]	DUMAT C, QUENEA K, BERMOND A, et al. Study of the trace metal ion influence on the turnover of soil organic matter in cultivated contaminated soils[J]. Environmental pollution, 2006, 142:521-529. pmid: 16338041
[33]	KLECZEK A, ANIELAK A M. Humic substances and significance of their application -a review[J]. Technical transactions, 2021,1-14.
[34]	SHAHID M, DUMA C, SILVESTRE J, et al. Effect of fulvic acids on lead-induced oxidative stress to metal sensitive Vicia faba L. plant[J]. Biology and fertility of soils, 2012, 48:689-697. doi: 10.1007/s00374-012-0662-9 URL
[35]	SANTOS N M, ACCIOLY A M A, NASCIMENTO C W A, et al. Humic acids and activated charcoal as soil amendments to reduce toxicity in soil contaminated by lead[J]. Revista brasileira de ciência do solo, 2014, 38:345-351. doi: 10.1590/S0100-06832014000100035 URL
[36]	MATUSZAK-SLAMANI R, BEJGER R, CIESLA J, et al. Influence of humic acid molecular fractions on growth and development of soybean seedlings under salt stress[J]. Plant growth regulation, 2017, 83:465-477. doi: 10.1007/s10725-017-0312-1
[37]	CWIELAG-PIASECKA I, MEDYNSKA-JURASZEK A, JERZYKIEWICZ M, et al. Humic acid and biochar as specific sorbents of pesticides[J]. Journal of soils and sediments, 2018, 18:2692-2702. doi: 10.1007/s11368-018-1976-5
[38]	ARAYA M, CORDOVA A, SAAVEDRA J, et al. Humic substances and their relation to pesticide sorption in eight volcanic soils[J]. Planta daninha, 2020, 38:1-11.
[39]	CHIANESE S, FENTI A, IOVINO P, et al. Sorption of organic pollutants by humic acids: a review[J]. Molecules, 2020, 25(4):918. doi: 10.3390/molecules25040918 URL
[40]	ROSA A H, OLIVEIR DE A L C, BELLIN I C, et al. Influence of alkaline extraction on the characteristics of humic substances in Brazilian soils[J]. Thermochimica acta, 2005, 433:77-82. doi: 10.1016/j.tca.2005.02.001 URL
[41]	SENESI N. Binding mechanisms of pesticides to soil humic substances[J]. Science of the total environment, 1992,123-124:63-76.
[42]	SENESI N, LOFFREDO E, Orazio V D, et al. Adsorption of pesticides by humic acids from organic amendments and soils. In: Humic substances and chemical contaminants[M]. Soil Science Society of America, Madison, WI, 2001:129-153.
[43]	SCHIAVON M, PIZZEGHELLO D, MUSCOLO A, et al. High molecular size humic substances enhance phenylpropanoid metabolismin maize (Zea mays L.)[J]. Journal of chemical ecology, 2010, 36:662-669. doi: 10.1007/s10886-010-9790-6 URL
[44]	HERNANDEZ O L, GARCIA A C, HUELVA R, et al. Humic substances from vermicompost enhance urban lettuce production[J]. Agronomy for sustainable development, 2015, 35:225-232. doi: 10.1007/s13593-014-0221-x URL
[45]	PEREIRA M M A, MORAIS L C, MARQUES E A, et al. Humic substances and efficient microorganisms:elicitation of medicinal plants-a review[J]. Journal of agricultural science, 2019, 11(7):268- 280. doi: 10.5539/jas.v11n7p268 URL
[46]	SAID-AL AHL H A H, GENDY EL A G, OMER E A. Humic acid and indole acetic acid affect yield and essential oil of dill grown under two different locations in Egypt[J]. International journal of pharmacy and pharmaceutical sciences, 2016, 8:146-157. doi: 10.22159/ijpps.2016v8i9.12664 URL
[47]	HAGHIGHI M, NIKBAKHT A, PESSARAKLI M. Effects of humic acid on remediation of the nutritional deficiency of gerbera in hydroponic culture[J]. Journal of plant nutrition, 2016:39.
[48]	CANELLASA L P, OLIVARESA F L, AGUIAR N O, et al. Humic and fulvic acids as biostimulants in horticulture[J]. Scientia horticulturae, 2015, 196 (30):15-27. doi: 10.1016/j.scienta.2015.09.013 URL
[49]	APEL K, HIRT H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction[J]. annual review of plant biology, 2004, 55:373-399. pmid: 15377225
[50]	KELLOS T, TIMAR I, SZILAGYI V, et al. Stress hormones and abiotic stresses have different effects on antioxidants in maize lines with different sensitivity[J]. Plant biology, 2008, 10:563-572. doi: 10.1111/j.1438-8677.2008.00071.x pmid: 18761495
[51]	CANELLAS L P, CANELLAS N O A, IRINEU L E S S, et al. Plant chemical priming by humic acids[J]. Chemical and biological technologies in agriculture, 2020, 7:12. doi: 10.1186/s40538-020-00178-4
[52]	PIZZEGHELLO D, NICOLINI G, NARDI S. Hormone-like activity of humic substances in Fagus sylvatica forests[J]. New phytologist, 2001, 151:647-657. doi: 10.1046/j.0028-646x.2001.00223.x URL
[53]	SUN J H, QIU C, DING Y Q, et al. Fulvic acid ameliorates drought stress-induced damage in tea plants by regulating the ascorbate metabolism and flavonoids biosynthesis[J]. BMC genomics, 2020, 21:411. doi: 10.1186/s12864-020-06815-4 pmid: 32552744
[54]	VASCONCELOS DE A C F. Amelioration of drought stress on plants under biostimulant sources[J]. Plant stress physiology, 2020, 1-14.
[55]	HOHMANN I, BILL R, KAYINGO I, et al. Microbial MIP channels[J]. Trends in microbiology, 2000, 8:33-38. pmid: 10637642
[56]	CORDEIRO F C, SANTA-CATARINA C, SILVEIRA V, et al. Humic acid effect on catalase activity and the generation of reactive oxygen species in corn (Zea mays L.)[J]. Bioscience, biotechnology, and biochemistry, 2011, 75:70-74. doi: 10.1271/bbb.100553 URL
[57]	ZAMANI A, KARIMI M, ABBASI-SURKI A, et al. The effect of humic acid application on stevia (Stevia rebaudiana) growth and metabolites under drought stress[J]. Iranian journal of plant physiology, 2021, 11(3):3651-3658.
[58]	YIGIDER E, TASPINAR M S, SIGMAZ B, et al. Humic acids protective activity against manganese induced LTR (long terminal repeat) retrotransposon polymorphism and genomic instability effects in Zea mays[J]. Plant gene, 2016, 6:13-17. doi: 10.1016/j.plgene.2016.03.002 URL
[59]	OLIVARES F L, BUSATO J G, PAULA DE A M, et al. Plant growth promoting bacteria and humic substances: crop promotion and mechanisms of action[J]. Chemical and biological technologies in agriculture, 2017, 4:30. doi: 10.1186/s40538-017-0112-x URL
[60]	DESOKY E S M, MERWAD A R M, RADY M M. Natural biostimulants improve saline soil characteristics and salt stressed-sorghum performance[J]. Communications in soil science and plant analysis, 2018, 49(8):67-83.
[61]	HATAMI E, ALI A S, ALI R G. Alleviating salt stress in almond rootstocks using of humic acid[J]. Scientia horticulturae, 2018, 237:296-302. doi: 10.1016/j.scienta.2018.03.034 URL
[62]	HEMIDA K A, ELOUFEY A Z A, SEIF EL-YAZAL M A, et al. Integrated effect of potassium humate and α-tocopherol applications on soil characteristics and performance of Phaseolus vulgaris plants grown on a saline soil[J]. Archives of agronomy and soil science, 2017, 63: 1556-1571. doi: 10.1080/03650340.2017.1292033 URL
[63]	BENAZZOUK S, DJAZOULI Z E, LUTTS S. Assessment of the preventive effect of vermicompost on salinity resistance in tomato (Solanum lycopersicum cv. Ailsa Craig)[J]. Acta physiologiae plantarum, 2018, 40:121. doi: 10.1007/s11738-018-2696-6
[64]	YILDIZTEKIN M, TUNA A L, KAYA C. Physiological effects of the brown seaweed (Ascophyllum nodosum) and humic substances on plant growth, enzyme activities of certain pepper plants grown under salt stress[J]. Acta biologica hungarica, 2018, 69(3):325-335. doi: 10.1556/018.68.2018.3.8 URL
[65]	KAYA C, AKRAM N A, ASHRAF M, et al. Exogenous application of humic acid mitigates salinity stress in maize (Zea mays L.) plants by improving some key physico-biochemical attributes[J]. Cereal research communications, 2018, 46(1):67-78. doi: 10.1556/0806.45.2017.064 URL
[66]	DINLER B S, GUNDUZER E, TEKINAY T. Pre-treatment of fulvic acid plays a stimulant role in protection of soybean (Glycine max L.) leaves against heat and salt stress[J]. Acta biologica cracoviensia. series botanica, 2016, 58/1:29-41.
[67]	RADY M M, ABD EL-MAGEED T A, ABDURRAHMAN H A, et al. Humic acid application improves field performance of cotton (Gossypium barbadense L. ) under saline conditions[J]. The journal of animal & plant sciences, 2016, 26(2):487-493.
[68]	DOBBSS L B, SANTOS T S C, PITTARELLO M, et al. Alleviation of iron toxicity in Schinus terebinthifolius Raddi (Anacardiaceae) by humic substances[J]. Environmental science and pollution research, 2018, 10:9416-9425.
[69]	PORTUONDO-FARIAS L, MARTINEZ-BALMORI D, IZQUIERDO-GURIDI F, et al. Structural and functional evaluation of humic acids in interaction with toxic metals in a cultivar of agricultural interest[J]. Revista ciencias técnicas agropecuarias, 2017, 26:39-46.
[70]	CHAAB A, MOEZZI A, SAYYAD G O, et al. Alleviation of cadmium toxicity to maize by the application of humic acid and compost[J]. Life science journal, 2016, 13(12):56-63.
[71]	BASAHI M. Humic acid improved germination rate, seedling growth and antioxidant system of pea (Pisum sativum L. var. Alicia) grown in water polluted with CdCl₂[J]. AIMS environmental science, 2021, 8(4):358-370. doi: 10.3934/environsci.2021023 URL
[72]	SERGIEV I, TODOROVA D, MOSKOVA I, et al. Protective effect of humic acids against heavy metal stress in triticale[J]. Comptes rendus de l’Academie bulgare des Sciences, 2013, 66(1):53-60.
[73]	DUAN D, TONG J, XU Q, et al. Regulation mechanisms of humic acid on Pb stress in tea plant (Camellia sinensis L.)[J]. Environmental pollution, 2020, 267:115546.
[74]	ALI S, BHARWANA S A, RIZWAN M, et al. Fulvic acid mediates chromium (Cr) tolerance in wheat (Triticum aestivum L.) through lowering of Cr uptake and improved antioxidant defense system[J]. Environmental science and pollution research, 2015, 22:10601-10609. doi: 10.1007/s11356-015-4271-7 URL
[75]	AGUIAR N O, MEDICI L O, OLIVARES F L, et al. Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria[J]. Annals of applied biology, 2016, 168:203-213. doi: 10.1111/aab.2016.168.issue-2 URL
[76]	BARZEGAR T, MORADI P, NIKBAKHT J, et al. Physiological response of Okra cv. Kano to foliar application of putrescine and humic acid under water deficit stress[J]. International journal of horticultural science and technology, 2016, 3(2):187-197.
[77]	LOTFI R, PESSARAKLI M, GHARAVI-KOUCHEBAGH P, et al. Physiological responses of Brassica napus to fulvic acid under water stress: chlorophyll a fluorescence and antioxidant enzyme activity[J]. The crop journal, 2015, 3:434-439. doi: 10.1016/j.cj.2015.05.006 URL
[78]	CHEN Q, QU Z M, MA G H, et al. Humic acid modulates growth, photosynthesis, hormone and osmolytes system of maize under drought conditions[J]. Agricultural water management, 2022, 263:107447.
[79]	GARCIA A C, SANTOS L A, GURIDI-IZQUIERDO F, et al. Potentialities of vermicompost humic acids to alleviate water stress in rice plants (Oryza sativa L.)[J]. Journal of geochemical exploration, 2014, 136:48-54. doi: 10.1016/j.gexplo.2013.10.005 URL
[80]	LOTFI R, KALAJI H M, VALIZADEH G R, et al. Effects of humic acid on photosynthetic efficiency of rapeseed plants growing under different watering conditions[J]. Photosynthetica, 2018, 56:962-970. doi: 10.1007/s11099-017-0745-9 URL
[81]	KRAN S, FURTANA G B, TALHOUNI M, et al. Drought stress mitigation with humic acid in two Cucumis melo L. genotypes differ in their drought tolerance[J]. Bragantia, 2019, 78(4):490-497. doi: 10.1590/1678-4499.20190057 URL
[82]	SHAH Z H, REHMAN H M, AKHTAR T, et al. Humic substances: determining potential molecular regulatory processes in plants[J]. Frontiers in plant science, 2018, 9:263. doi: 10.3389/fpls.2018.00263 pmid: 29593751
[83]	UDVARDI M, POOLE P S. Transport and metabolism in legume-rhizobia symbioses[J]. Annual review of plant biology, 2013, 64:781-805. doi: 10.1146/annurev-arplant-050312-120235 pmid: 23451778
[84]	NARDI S, ERTANI A, ORNELLA F. Soil-root cross-talking: the role of humic substances[J]. Journal of plant nutrition and soil science, 2017, 180:5-13. doi: 10.1002/jpln.v180.1 URL
[85]	MELO R O, OLIVEIRA H P, SILVEIRA K C, et al. Initial performance of maize in response to humic acids and plant growth-promoting bacteria[J]. Revista ceres, 2018, 65(3):271-277. doi: 10.1590/0034-737x201865030007 URL
[86]	LIMA L S, OLIVARES F L, OLIVEIRA R R, et al. Root exudate profiling of maize seedlings inoculated with Herbaspirillum seropedicae and humic acids[J]. Chemical and biological technologies in agriculture, 2014, 1:23. doi: 10.1186/s40538-014-0023-z URL
[87]	JAMES E K, OLIVARES F L. Infection and colonization of sugarcane and other graminaceous plants by endophytic diazotrophs[J]. Critical reviews in plant sciences, 1998, 17:77-119. doi: 10.1080/07352689891304195 URL
[88]	OLIVARES F L, AGUIAR N O, ROSA R C C, et al. Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes[J]. Scientia horticulturae, 2015, 183:100-108. doi: 10.1016/j.scienta.2014.11.012 URL
[89]	GHORBANPOUR M, HATAMI M. Biopriming of salvia officinalis seed with growth promoting rhizobacteria affects invigoration and germination Indices[J]. Journal of biological and environmental sciences, 2014, 8(22):29-36.
[90]	GRYNDLER M, HRSELOVA H, SUDOVA R, et al. Hyphal growth and mycorrhiza formation by the arbuscular mycorrhizal fungus Glomus claroideum BEG 23 is stimulated by humic substances[J]. Mycorrhiza, 2005, 15:483-488. doi: 10.1007/s00572-005-0352-7 URL
[91]	FALLAHI H R, GHORBANY M, SAMADZADEH A, et al. Influence of arbuscular mycorrhizal inoculation and humic acid application on growth and yield of roselle (Hibiscus sabdariffa L.) and its mycorrhizal colonization index under deficit irrigation[J]. International journal of horticultural science and technology, 2016, 3(2):113-128.
[92]	HASHEMZADEH F, MIRSHEKARI B, KHOEI F R, et al. Effect of bio and chemical fertilizers on seed yield and its components of dill (Anethum graveolens)[J]. Journal of medicinal plants research, 2013, 7:111-117.
[93]	BHARTI N, BARNAWAL D, SHUKLA S, et al. Integrated application of Exiguobacterium oxidotolerans, Glomus fasciculatum, and vermicompost improves growth, yield and quality of Mentha arvensis in salt-stressed soils[J]. Industrial crops and products, 2016, 83:717-728. doi: 10.1016/j.indcrop.2015.12.021 URL

非生物胁迫	供试植物		HS	生物活性物质的产生	抗氧化活性	参考文献
盐胁迫	辣木		HS	光合色素，脯氨酸，可溶性糖，抗坏血酸，谷胱甘肽等	CAT, POX	[60]
	扁桃		HA	可溶性蛋白	CAT, POX	[61]
	菜豆		HA	脯氨酸，可溶性糖，抗坏血酸	CAT, SOD,GPOX	[62]
	番茄		堆肥	可溶性糖	-	[63]
	泡叶藻		HS	脯氨酸	SOD, CAT, POX	[64]
	玉米		HA	脯氨酸	SOD, POD, CAT	[65]
	大豆		FA	MDA，H₂O₂	SOD, APX, GST	[66]
	海岛棉		HA	脯氨酸，游离糖	-	[67]
重金属胁迫	巴西胡椒木		HS/Fe	脯氨酸	CAT, SOD, POX	[68]
	菜豆		HA/Pb	脯氨酸	CAT, SOD, POX	[69]
	玉米		HA/Cd 堆肥	脯氨酸	SOD, CAT	[70]
	豌豆		HA/Cd	-	POX	[71]
	小黑麦		HA/Cu, Cd	脯氨酸	SOD, CAT, GPOX, GST	[72]
	茶		HA/Pb	MAD	-	[73]
	小麦		FA/Cr	总叶绿素，类胡萝卜素，可溶性蛋白	CAT, 抗坏血酸	[74]
干旱胁迫		茶树	FA	抗坏血酸、谷胱甘肽、类黄酮	-	[36]
		甘蔗.	HA	碳水化合物，蛋白质，芳族化合物	CAT, POX, SOD	[75]
		秋葵	HA	脯氨酸，维生素c	CAT, POX	[76]
		油菜	FA	脯氨酸	CAT, POX, APX	[77]
		玉米	HA	可溶性糖、甜菜碱和脯氨酸	-	[78]
		水稻	HA	脯氨酸	POX	[79]
		油菜	HA	叶绿素a	-	[80]
		哈密瓜	HA	叶绿素	SOD, CAT, GR	[81]

非生物胁迫	供试植物		HS	生物活性物质的产生	抗氧化活性	参考文献
盐胁迫	辣木		HS	光合色素，脯氨酸，可溶性糖，抗坏血酸，谷胱甘肽等	CAT, POX	[60]
	扁桃		HA	可溶性蛋白	CAT, POX	[61]
	菜豆		HA	脯氨酸，可溶性糖，抗坏血酸	CAT, SOD,GPOX	[62]
	番茄		堆肥	可溶性糖	-	[63]
	泡叶藻		HS	脯氨酸	SOD, CAT, POX	[64]
	玉米		HA	脯氨酸	SOD, POD, CAT	[65]
	大豆		FA	MDA，H₂O₂	SOD, APX, GST	[66]
	海岛棉		HA	脯氨酸，游离糖	-	[67]
重金属胁迫	巴西胡椒木		HS/Fe	脯氨酸	CAT, SOD, POX	[68]
	菜豆		HA/Pb	脯氨酸	CAT, SOD, POX	[69]
	玉米		HA/Cd 堆肥	脯氨酸	SOD, CAT	[70]
	豌豆		HA/Cd	-	POX	[71]
	小黑麦		HA/Cu, Cd	脯氨酸	SOD, CAT, GPOX, GST	[72]
	茶		HA/Pb	MAD	-	[73]
	小麦		FA/Cr	总叶绿素，类胡萝卜素，可溶性蛋白	CAT, 抗坏血酸	[74]
干旱胁迫		茶树	FA	抗坏血酸、谷胱甘肽、类黄酮	-	[36]
		甘蔗.	HA	碳水化合物，蛋白质，芳族化合物	CAT, POX, SOD	[75]
		秋葵	HA	脯氨酸，维生素c	CAT, POX	[76]
		油菜	FA	脯氨酸	CAT, POX, APX	[77]
		玉米	HA	可溶性糖、甜菜碱和脯氨酸	-	[78]
		水稻	HA	脯氨酸	POX	[79]
		油菜	HA	叶绿素a	-	[80]
		哈密瓜	HA	叶绿素	SOD, CAT, GR	[81]