腐植酸促进作物根系生长机理的研究进展
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摘要
腐植酸对植物根系生长的刺激作用是其对植物生长促进作用的最初动力。从腐植酸对作物根系形态、养分吸收、基因表达及根际微生物的影响方面,阐述腐植酸对根系的刺激机理与影响的关键因子,总结腐植酸促进根系生长的研究现状,为腐植酸的进一步开发利用提供理论依据。主要进展如下:(1)腐植酸能从细胞水平和根构型来影响根系形态;(2)腐植酸能刺激根伸长、增加根密度与表面积,促进养分吸收;(3)腐植酸可通过诱导增加质膜H~+-ATP酶量、酸化内质体、松动细胞壁、促进细胞伸长等来影响根系活动;(4)腐植酸可影响根际微生物的种类和数量,从而调节与土壤之间的互作关系以改善根系活动;(5)腐植酸对作物根系的作用效果受其来源、浓度、分子量、官能团、结构和成分的影响。目前关于腐植酸的研究技术水平有限,关于腐植酸对根系的研究多集中于某一阶段,因此后续如何采用非破坏性手段研究腐植酸,以及系统研究腐植酸对根系作用机理,值得进一步深入。
The stimulating effect of humic acid on plant root growth is its initial driving force for plant growth. In this paper, the effects of humic acid on root morphology, nutrient uptake, gene expression and rhizosphere microbes were discussed and the key factors of humic acid on root stimulation mechanism and influence were set forth. The research status of humic acid to promote root growth was also summarized in order to provide a theoretical basis for further development and utilization:(1) Humic acid can cause root morphology by changing root cell and root systematic architecture;(2) Humic acid can stimulate root elongation, increase root density and surface area, and promote nutrient absorption;(3) Humic acid can induce the increase of plasma membrane H~+-ATPase, acidify endosome, loosen cell wall, and promote cell elongation to affect root activity;(4) The species and quantity of rhizosphere microorganisms can be changed by humic acids to regulate the interaction with the soil to improve root activity;(5) The effect of humic acid on crop roots is influenced by its source, concentration, molecular weight, functional group, structure and composition.At present, the research methods on humic acid are not sufficient. It is necessary to use non-destructive method to study humic acid and the mechanism of humic acid on crop roots of the entire growth cycle.
The stimulating effect of humic acid on plant root growth is its initial driving force for plant growth. In this paper, the effects of humic acid on root morphology, nutrient uptake, gene expression and rhizosphere microbes were discussed and the key factors of humic acid on root stimulation mechanism and influence were set forth. The research status of humic acid to promote root growth was also summarized in order to provide a theoretical basis for further development and utilization:(1) Humic acid can cause root morphology by changing root cell and root systematic architecture;(2) Humic acid can stimulate root elongation, increase root density and surface area, and promote nutrient absorption;(3) Humic acid can induce the increase of plasma membrane H~+-ATPase, acidify endosome, loosen cell wall, and promote cell elongation to affect root activity;(4) The species and quantity of rhizosphere microorganisms can be changed by humic acids to regulate the interaction with the soil to improve root activity;(5) The effect of humic acid on crop roots is influenced by its source, concentration, molecular weight, functional group, structure and composition.At present, the research methods on humic acid are not sufficient. It is necessary to use non-destructive method to study humic acid and the mechanism of humic acid on crop roots of the entire growth cycle.
引文
[1]郑平.煤炭腐植酸的生产和应用[M].北京:化学工业出版社,1991:28.
[2] Calvo P, Nelson L,Kloepper J W. Agricultural uses of plant biostimulants[J]. Plant&Soil,2014, 383(1-2):3-41.
[3] Vaughan D, Malcolm R E. Influence of humic substances on growth and physiological processes[M]//Soil organic matter and biological activity. Springer, Dordrecht, 1985:37-75.
[4] Canellas L P, Olivares F L, Okorokova-Facanha A L, et al.Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots[J]. Plant physiology,2002, 130(4):1951-1957.
[5] Zandonadi D B, Canellas L P, Facanha A R. Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+pumps activation[J]. Planta,2007, 225(6):1583-1595.
[6] Schmidt W, Santi S, Pinton R, et al. Water-extractable humic substances alter root development and epidermalcell pattern in Arabidopsis[J]. Plant and Soil, 2007,300(1-2):259-267.
[7] Pinton R, Cesco S, Iacolettig G, et al. Modulation of NO3-uptake by water-extractable humic substances:involvement of root plasma membrane H+-ATPase[J].Plant and soil,1999, 215(2):155-161.
[8] Canellas L P,Piccolo A,Dobbss L B, et al. Chemical composition and bioactivity properties of sizefractions separated from a vermicompost humic acid[J].Chemosphere,2010, 78(4):457-466.
[9] Dobbss L B,Medici L O, Peres L E P,et al. Changes in root development of Arabidopsis promoted by organic matter from oxisols[J]. Annals of Applied Biology, 2007,151(2):199-211.
[10] Dobbss L B,Pasqualoto C L,Lopes O F,et al. Bioactivity of chemically transformed humic matter from vermicompost on plant root growth[J]. Journal of Agricultural and Food Chemistry,2010, 58(6):3681-3688.
[11] Trevisan S, Pizzeghello D, Ruperti B, et al. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5synthetic element in Arabidopsis[J]. Plant Biology, 2010,12(4):604-614.
[12] Chen Y, Aviad T. Effects of humic substances on plant growth[M]//Humic substances in soil and crop sciences:selected readings. Soil Science Society of America,1990:161-186.
[13] Varanini Z, Pinton R. Humic substances and plant nutrition[M]. Heidelberg:Springer Berli, 1995.
[14] Uphoff N, Ball A S, Fernandes E, et al. Biological approaches to sustainable soil systems[M]. Boca Raton:CRC Press, 2006.
[15] Tattini M, Bertoni P, Landi A, et al. Effect of humic acids on growth and biomass partitioning of container-grown olive plants[C].ⅡSymposium on horticultural substrates and their analysis.ⅩⅩⅢIHC 294, 1990:75-80.
[16] Orlova O V, Arkhipchenko I A. Humic substances of composts from municipal solid wastes as a promising plant growth stimulator[J]. Russian AgriculturalSciences,2009, 35(3):175-178.
[17] Eyheraguibel B, Silvestre J, Morard P. Effects of humic substances derived from organic waste enhancement on the growth and mineral nutrition of maize[J]. Bioresource technology,2008, 99(10):4206-4212.
[18] Garcia C,Hernandez T,Pascual J A, et al. Microbial activity in soils of SE Spain exposed to degradation and desertification processes. Strategies for their rehabilitation[M]//Research and perspectives of soil enzymology in Spain. Spain:CEBAS-CSIC, 2000.
[19]梅慧生,杨玉明,张淑运,等.腐殖酸钠对植物生长的刺激作用[J].植物生理学报,1980(2):30-37.
[20]周霞萍,邓林,韩媛媛,等.腐植酸天然植物生长素调节剂[J].中国生物防治,2006(S1):163-170.
[21] Sanchez C, Vielba J M, Ferro E, et al. Two SCARECROW-LIKE genes are induced in response to exogenous auxin in rooting-competent cuttings of distantly related forest species[J]. Tree physiology, 2007,27(10):1459-1470.
[22] Heo J O, Chang K S, Kim I A, et al. Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root[J].Proceedings of the National Academy of Sciences, 2011,108(5):2166-2171.
[23]张丽丽,刘德兴,史庆华,等.黄腐酸对番茄幼苗适应低磷胁迫的生理调控作用[J].中国农业科学,2018, 51(8):1547-1555.
[24] Varanini Z, Pinton R,De Biasi M G, et al. Low molecular weight humic substances stimulate H+-ATPase activity of plasma membrane vesicles isolated from oat(Avena sativa L.)roots[J]. Plant and soil, 1993, 153(1):61-69.
[25] Nardi S, Concheri G, Pizzeghello D, et al. Soil organic matter mobilization by root exudates[J]. Chemosphere,2000, 41(5):653-658.
[26] Tahiri A, Delporte F, Muhovski Y, et al. Change in ATPbinding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn inresponse to leachate and leonardite humic substances[J].Plant Physiology and Biochemistry,2016, 98:25-38.
[27] 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(4):2587-2596.
[28] Visser M. An exotic class of Kaluza-Klein models[J].Physics Letters B,1985, 159(1):22-25.
[29] Kulikova N A, Perminova I V, Badun G A, 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 environmental microbiology,2010, 76(18):6223-6230.
[30] Dong L, Cordova-Kreylos A L, Yang J, et al. Humic acids buffer the effects of urea on soil ammonia oxidizers and potential nitrification[J]. Soil Biology and Biochemistry,2009, 41(8):1612-1621.
[31] Puglisi E,Pascazio S, Suciu N,et al. Rhizosphere microbial diversity as influenced by humic substance amendments and chemical composition of rhizodeposits[J]. Journal of Geochemical Exploration,2013, 129:82-94.
[32] Bollmann A, Laanbroek H J. Continuous culture enrichments of ammonia-oxidizing bacteria at low ammonium concentrations[J]. FEMS Microbiology Ecology,2001,37(3):211-221.
[33] Mackowiak C L,Grossl P R,Bugbee B G. Beneficial effects of humic acid on micronutrient availability to wheat[J]. Soil Science Society of America Journal, 2001,65(6):1744-1750.
[34] Pertusatti J, Prado A G S. Buffer capacity of humic acid:thermodynamic approach[J]. Journal of colloid and interface science, 2007, 314(2):484-489.
[35]王利宾,王曰鑫.腐植酸肥对土壤养分与微生物活性的影响[J].腐植酸,2011(4):6-9.
[36] Canellas L P, Dobbss L B, Oliveira A L, et al. Chemical properties of humic matter as related to induction of plantlateral roots[J]. European Journal of Soil Science, 2012,63(3):315-324.
[37] Jindo K, Martim S A, Navarro E C, et al. Root growth promotion by humic acids from composted and noncomposted urban organic wastes[J]. Plant and Soil, 2012,353(1-2):209-220.
[38] Piccolo A,Nardi S, Concheri G. Structural characteristics of humic substances as related to nitrate uptake and growth regulation in plant systems[J]. Soil Biology and Biochemistry, 1992, 24(4):373-380.
[39] Nardi S,Pizzeghello D, Muscolo A,et al. Effects of forest humus on biological activity in roots of Pinus sylvestris related to chemical humus fraction characteristics[J]. Fresenius Environmental Bulletin,1998, 7(3-4):203-208.
[40] Nardi S, Pizzeghello D, Reniero F, et al. Chemical and biochemical properties of humic substances isolated from forest soils and plant growth[J]. Soil Science Society of America,2000, 64:639-645.
[41] Canellas L P, Faganha A R. Chemical nature of soil humified fractions and their bioactivity[J]. Pesquisa Agropecuaria Brasileira,2004, 39(3):233-240.
[42] Maggioni A, Varanini Z, Nardi S, et al. Action of soil humic matter on plant roots:stimulation of ion uptake and effects on(Mg2++K+)ATPase activity[J]. Science of the Total Environment,1987, 62:355-363.
[43] Albuzio A, Ferrari G, Nardi S. Effects of humic substances on nitrate uptake and assimilation in barley seedlings[J]. Canadian Journal of Soil Science, 1986,66(4):731-736.
[44] Yazawa Y,Wong M T F,Gilkes R J,et al. Effect of additions of brown coal and peat on soil solution composition and root growth in acid soil from wheatbelt of Western Australia[J]. Communications in Soil Science and Plant Analysis,2000, 31(5-6):743-758.
[45] David J, Smejkalova D, Hudecova S, et al. The physicochemical properties and biostimulative activities of humic substances regenerated from lignite[J]. SpringerPlus,2014,3(1):156.
[2] Calvo P, Nelson L,Kloepper J W. Agricultural uses of plant biostimulants[J]. Plant&Soil,2014, 383(1-2):3-41.
[3] Vaughan D, Malcolm R E. Influence of humic substances on growth and physiological processes[M]//Soil organic matter and biological activity. Springer, Dordrecht, 1985:37-75.
[4] Canellas L P, Olivares F L, Okorokova-Facanha A L, et al.Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots[J]. Plant physiology,2002, 130(4):1951-1957.
[5] Zandonadi D B, Canellas L P, Facanha A R. Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+pumps activation[J]. Planta,2007, 225(6):1583-1595.
[6] Schmidt W, Santi S, Pinton R, et al. Water-extractable humic substances alter root development and epidermalcell pattern in Arabidopsis[J]. Plant and Soil, 2007,300(1-2):259-267.
[7] Pinton R, Cesco S, Iacolettig G, et al. Modulation of NO3-uptake by water-extractable humic substances:involvement of root plasma membrane H+-ATPase[J].Plant and soil,1999, 215(2):155-161.
[8] Canellas L P,Piccolo A,Dobbss L B, et al. Chemical composition and bioactivity properties of sizefractions separated from a vermicompost humic acid[J].Chemosphere,2010, 78(4):457-466.
[9] Dobbss L B,Medici L O, Peres L E P,et al. Changes in root development of Arabidopsis promoted by organic matter from oxisols[J]. Annals of Applied Biology, 2007,151(2):199-211.
[10] Dobbss L B,Pasqualoto C L,Lopes O F,et al. Bioactivity of chemically transformed humic matter from vermicompost on plant root growth[J]. Journal of Agricultural and Food Chemistry,2010, 58(6):3681-3688.
[11] Trevisan S, Pizzeghello D, Ruperti B, et al. Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5synthetic element in Arabidopsis[J]. Plant Biology, 2010,12(4):604-614.
[12] Chen Y, Aviad T. Effects of humic substances on plant growth[M]//Humic substances in soil and crop sciences:selected readings. Soil Science Society of America,1990:161-186.
[13] Varanini Z, Pinton R. Humic substances and plant nutrition[M]. Heidelberg:Springer Berli, 1995.
[14] Uphoff N, Ball A S, Fernandes E, et al. Biological approaches to sustainable soil systems[M]. Boca Raton:CRC Press, 2006.
[15] Tattini M, Bertoni P, Landi A, et al. Effect of humic acids on growth and biomass partitioning of container-grown olive plants[C].ⅡSymposium on horticultural substrates and their analysis.ⅩⅩⅢIHC 294, 1990:75-80.
[16] Orlova O V, Arkhipchenko I A. Humic substances of composts from municipal solid wastes as a promising plant growth stimulator[J]. Russian AgriculturalSciences,2009, 35(3):175-178.
[17] Eyheraguibel B, Silvestre J, Morard P. Effects of humic substances derived from organic waste enhancement on the growth and mineral nutrition of maize[J]. Bioresource technology,2008, 99(10):4206-4212.
[18] Garcia C,Hernandez T,Pascual J A, et al. Microbial activity in soils of SE Spain exposed to degradation and desertification processes. Strategies for their rehabilitation[M]//Research and perspectives of soil enzymology in Spain. Spain:CEBAS-CSIC, 2000.
[19]梅慧生,杨玉明,张淑运,等.腐殖酸钠对植物生长的刺激作用[J].植物生理学报,1980(2):30-37.
[20]周霞萍,邓林,韩媛媛,等.腐植酸天然植物生长素调节剂[J].中国生物防治,2006(S1):163-170.
[21] Sanchez C, Vielba J M, Ferro E, et al. Two SCARECROW-LIKE genes are induced in response to exogenous auxin in rooting-competent cuttings of distantly related forest species[J]. Tree physiology, 2007,27(10):1459-1470.
[22] Heo J O, Chang K S, Kim I A, et al. Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root[J].Proceedings of the National Academy of Sciences, 2011,108(5):2166-2171.
[23]张丽丽,刘德兴,史庆华,等.黄腐酸对番茄幼苗适应低磷胁迫的生理调控作用[J].中国农业科学,2018, 51(8):1547-1555.
[24] Varanini Z, Pinton R,De Biasi M G, et al. Low molecular weight humic substances stimulate H+-ATPase activity of plasma membrane vesicles isolated from oat(Avena sativa L.)roots[J]. Plant and soil, 1993, 153(1):61-69.
[25] Nardi S, Concheri G, Pizzeghello D, et al. Soil organic matter mobilization by root exudates[J]. Chemosphere,2000, 41(5):653-658.
[26] Tahiri A, Delporte F, Muhovski Y, et al. Change in ATPbinding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn inresponse to leachate and leonardite humic substances[J].Plant Physiology and Biochemistry,2016, 98:25-38.
[27] 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(4):2587-2596.
[28] Visser M. An exotic class of Kaluza-Klein models[J].Physics Letters B,1985, 159(1):22-25.
[29] Kulikova N A, Perminova I V, Badun G A, 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 environmental microbiology,2010, 76(18):6223-6230.
[30] Dong L, Cordova-Kreylos A L, Yang J, et al. Humic acids buffer the effects of urea on soil ammonia oxidizers and potential nitrification[J]. Soil Biology and Biochemistry,2009, 41(8):1612-1621.
[31] Puglisi E,Pascazio S, Suciu N,et al. Rhizosphere microbial diversity as influenced by humic substance amendments and chemical composition of rhizodeposits[J]. Journal of Geochemical Exploration,2013, 129:82-94.
[32] Bollmann A, Laanbroek H J. Continuous culture enrichments of ammonia-oxidizing bacteria at low ammonium concentrations[J]. FEMS Microbiology Ecology,2001,37(3):211-221.
[33] Mackowiak C L,Grossl P R,Bugbee B G. Beneficial effects of humic acid on micronutrient availability to wheat[J]. Soil Science Society of America Journal, 2001,65(6):1744-1750.
[34] Pertusatti J, Prado A G S. Buffer capacity of humic acid:thermodynamic approach[J]. Journal of colloid and interface science, 2007, 314(2):484-489.
[35]王利宾,王曰鑫.腐植酸肥对土壤养分与微生物活性的影响[J].腐植酸,2011(4):6-9.
[36] Canellas L P, Dobbss L B, Oliveira A L, et al. Chemical properties of humic matter as related to induction of plantlateral roots[J]. European Journal of Soil Science, 2012,63(3):315-324.
[37] Jindo K, Martim S A, Navarro E C, et al. Root growth promotion by humic acids from composted and noncomposted urban organic wastes[J]. Plant and Soil, 2012,353(1-2):209-220.
[38] Piccolo A,Nardi S, Concheri G. Structural characteristics of humic substances as related to nitrate uptake and growth regulation in plant systems[J]. Soil Biology and Biochemistry, 1992, 24(4):373-380.
[39] Nardi S,Pizzeghello D, Muscolo A,et al. Effects of forest humus on biological activity in roots of Pinus sylvestris related to chemical humus fraction characteristics[J]. Fresenius Environmental Bulletin,1998, 7(3-4):203-208.
[40] Nardi S, Pizzeghello D, Reniero F, et al. Chemical and biochemical properties of humic substances isolated from forest soils and plant growth[J]. Soil Science Society of America,2000, 64:639-645.
[41] Canellas L P, Faganha A R. Chemical nature of soil humified fractions and their bioactivity[J]. Pesquisa Agropecuaria Brasileira,2004, 39(3):233-240.
[42] Maggioni A, Varanini Z, Nardi S, et al. Action of soil humic matter on plant roots:stimulation of ion uptake and effects on(Mg2++K+)ATPase activity[J]. Science of the Total Environment,1987, 62:355-363.
[43] Albuzio A, Ferrari G, Nardi S. Effects of humic substances on nitrate uptake and assimilation in barley seedlings[J]. Canadian Journal of Soil Science, 1986,66(4):731-736.
[44] Yazawa Y,Wong M T F,Gilkes R J,et al. Effect of additions of brown coal and peat on soil solution composition and root growth in acid soil from wheatbelt of Western Australia[J]. Communications in Soil Science and Plant Analysis,2000, 31(5-6):743-758.
[45] David J, Smejkalova D, Hudecova S, et al. The physicochemical properties and biostimulative activities of humic substances regenerated from lignite[J]. SpringerPlus,2014,3(1):156.
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