The mechanisms of fiber flax adaptation to high soil acidity (a review)
https://doi.org/10.30901/2227-8834-2020-4-205-212
Abstract
About the Authors
N. V. KishlyanRussian Federation
42, 44 Bolshaya Morskaya Street, St. Petersburg 190000
N. V. Melnikova
Russian Federation
32 Vavilova St., Moscow 119991
T. A. Rozhmina
Russian Federation
35 Lunacharskogo St., Torzhok 172002
References
1. Adenot X., Elmayan T., Lauressergues D., Boutet S., Bouché N., Gasciolli V. et al. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Current Biology. 2006;16(9):927-932. DOI: 10.1016/j.cub.2006.03.035
2. Allen E., Xie Z., Gustafson A.M., Carrington J.C. microRNAdirected phasing during trans-acting siRNA biogenesis in plants. Cell. 2005;121(2):207-221. DOI: 10.1016/j.cell.2005.04.004
3. Amosova N.V., Nikolaeva O.N., Synzynys B.I. Mechanisms of aluminum tolerance in cultivated plants (review). Agricultural Biology. 2007;42(1):36-42. [in Russian]
4. Avdonin N.S. Increasing fertility of acidic soils (Povysheniye plodorodiya kislykh pochv). Moscow: Kolos; 1969. [in Russian]
5. Axtell M.J., Jan C., Rajagopalan R., Bartel D.P. A two-hit trigger for siRNA biogenesis in plants. Cell. 2006;127(3):565- 577. DOI: 10.1016/j.cell.2006.09.032
6. Axtell M.J., Westholm J.O., Lai E.C. Vive la différence: Biogenesis and evolution of microRNAs in plants and animals. Genome Biology. 2011;12(4):221. DOI: 10.1186/gb-2011-12-4-221
7. Bose J., Babourina O., Shabala S., Rengel Z. Low-pH and aluminum resistance in Arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant and Cell Physiology. 2013;54(7):1093-1104. DOI: 10.1093/pcp/pct064
8. Cançado G.M.A., De Rosa Jr. V.E., Fernandez J.H., Maron L.G., Jorge R.A., Menossi M. Glutathione S-transferase and aluminum toxicity in maize. Functional Plant Biology. 2005;32(11):1045-1055. DOI: 10.1071/fp05158
9. Chen L., Wang T., Zhao M., Tian Q., Zhang W.H. Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta. 2012;235(2):375-386. DOI: 10.1007/s00425-011-1514-9
10. Chen Q., Zhang X.D., Wang S.S., Wang Q.F., Wang G.Q., Nian H.J. et al. Transcriptional and physiological changes of alfalfa in response to aluminium stress. The Journal of Agricultural Science. 2011;149(6):737-751. DOI: 10.1017/S0021859611000256
11. Dmitriev A.A., Krasnov G.S., Rozhmina T.A., Kishlyan N.V., Zyablitsin A.V., Sadritdinova A.F. et al. Glutathione S-transferases and UDP-glycosyltransferases are involved in response to aluminum stress in flax. Frontiers in Plant Science. 2016; 7:1920. DOI: 10.3389/fpls.2016.01920
12. Dmitriev A.A., Kudryavtseva A.V., Bolsheva N.L., Zyabli tsin A.V., Rozhmina T.A., Kishlyan N.V. et al. MiR319, miR390, and miR393 are involved in aluminum response in flax (Linum usitatissimum L.). BioMed Research International. 2017;2017:4975146. DOI: 10.1155/2017/4975146
13. Ezaki B., Gardner R.C., Ezaki Y., Matsumoto H. Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiology 2000;122(3):657-665. DOI: 10.1104/pp.122.3.657
14. Fahlgren N., Montgomery T.A., Howell M.D., Allen E., Dvorak S.K., Alexander A.L. et al. Regulation of AUXIN RESPONSE FACTOR 3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Current Biology. 2006;16(9):939-944. DOI: 10.1016/j.cub.2006.03.065
15. Foy C.D. Physiological effects of hydrogen, aluminum, and manganese toxicities in acid soil. In: F. Adams (ed.). Soil acidity and liming. Madison, Wisconsin: American Society of Agronomy; 1984. p.57-97.
16. Foy C.D. Tolerance of barley cultivars to an acid, aluminumtoxic subsoil related to mineral element concentration in their shoots. Journal of Plant Nutrition. 1996;19(10- 11):1361-1380. DOI: 10.1080/01904169609365205
17. Foyer C.H., Noctor G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell. 2005;17(7):1866-1875. DOI: 10.1105/tpc.105.033589
18. Gill G.W., Frost J.K, Miller K.A. A new formula for a half-oxidized hematoxylin solution that neither overstains nor requires differentiation. Acta Cytologica. 1974;18(4):300-311.
19. Gоrdeev A.V. (ed.) Bioclimatic potential of Russia: productivity and rational placement of agricultural crops in the conditions of climate change (Bioklimaticheskiy potentsial Rossii: produktivnost i ratdionalnoye razmeshcheniye selskokhozyaystvennykh kultur v usloviyakh izmeneniya klimata). Moscow: Ministry of Agriculture of the Russian Federation; 2012. [in Russian]
20. Goulding K.W.T. Soil acidification and the importance of liming agricultural soils with particular reference to the United Kingdom. Soil Use and Management. 2016;32(3):390-399. DOI: 10.1111/sum.12270
21. Grevenstuk T., Romano A. Aluminium speciation and internal detoxification mechanisms in plants: where do we stand? Metallomics. 2013;5(12):1584-1594. DOI: 10.1039/c3mt00232b
22. Guo J.H., Liu X.J., Zhang Y., Shen J.L., Han W.X., Zhang W.F. et al. Significant acidification in major Chinese croplands. Science. 2010;327(5968):1008-1010. DOI: 10.1126/science.1182570
23. Hasanuzzaman M., Hossain M.A., da Silva J.A.T., Fujita M. Plant response and tolerance to abiotic oxidative stress: Antioxidant defense is a key factor. In: B. Venkateswarlu., A.K. Shanker, C. Shanker, M. Maheswari (eds). Crop Stress and Its Management: Perspectives and Strategies. Dordrecht: Springer; 2012. pp.261-315.
24. Hasanuzzaman M., Nahar K., Anee T.I., Fujita M. Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants. 2017;23(2):249-268. DOI: 10.1007/s12298-017-0422-2
25. He H., He L., Gu M. Role of microRNAs in aluminum stress in plants. Plant Cell Reports. 2014;33(6):831-836. DOI: org/10.1007/s00299-014-1565-z
26. Huang Y., Wang J.P., Yu X.L., Wang Z.V., Xu T.S., Cheng X.C. Non-coding RNAs and diseases. Molecular Biology. 2013;47(4):531-544. [in Russian]. DOI: 10.7868/S0026898413040174
27. Jones D.L., Blancaflor E.B., Kochian L.V., Gilroy S. Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant, Cell and Environment. 2006;29(7):1309-1318. DOI: 10.1111/j.1365-3040.2006.01509.x
28. Jones-Rhoades M.W., Bartel D.P., Bartel B. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology. 2006;57:19-53. DOI: 10.1146/annurev.arplant.57.032905.105218
29. Kalinina E.V., Chernov N.N., Novichkova M.D. The role of glutathione, glutathionetransferase and glutaredoxin in the regulation of redox-dependent processes. (Rol glutationa, glutationtransferazy i glutaredoksina v regulyatsii redoks-zavisimykh protsessov). Uspekhi biologicheskoy khimii = Advances in Biological Chemistry. 2014;54:299-348. [in Russian]
30. Kikui S., Sasaki T., Maekawa M., Miya A., Hirochika H., Matsumoto H. et al. Physiological and genetic analyses of aluminum tolerance in rice, focusing on root growth during germination. Journal of Inorganic Biochemistry. 2005;99(9):1837-1844. DOI: org/10.1016/j.jinorgbio.2005.06.031
31. Kinraide T.B. Identity of the rhizotoxic aluminium species. Plant and Soil. 1991;134(1):167-178. DOI: 10.1007/bf00010729
32. Kishlyan N.V., Rozhmina T.A. Investigation of flax (Linum usitatissimum L.) gene pool on resistance to soil acidity. Agricultural. Biology. 2010;1:96-103. [in Russian].
33. Kishlyan N.V., Rozhmina T.A., Nikitinskaya T.V., Titok V.V. Influence of soil acidity on productivity and fiber quality of fiber flax accessions (Vliyaniye kislotnosti pochvy na produktivnost i kachestvo volokna obraztsov lna-dolguntsa). In: I.A. Golub (ed.). Flax Growing: Realities and Prospects (Lnovodstvo: realii i perspektivy). Proceedings of the International Scientific and Practical Conference (Ustye Village, Orsha District, Vitebsk Province, June 25–28, 2008). Mogilev, Belarus; 2008. p.131-140. [in Russian]
34. Kisseljov F.L. MicroRNAs and cancer. Molecular Biology. 2014;48(2):232-242. [in Russian] DOI: 10.7868/S0026898414020086
35. Klimashevsky E.L. Genetic aspect of mineral nutrition of plants. (Geneticheskiy aspekt mineralnogo pitaniya rasteniy). Moscow: Agropromizdat; 1991. [in Russian]
36. Klimashevsky E.L., Markova Yu.A., Sabirova R.N. About the nature of the genotypic specificity of plant resistance to aluminum (O prirode genotipicheskoy spetsifiki ustoychivosti rasteniy k alyuminiyu). Doklady VASKhNIL = Reports of VASKhNIL. 1978;8:2-5. [in Russian]
37. Kochian L.V, Hoekenga O.A., Piñeros M.A. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology 2004;55(1):459-493. DOI: 10.1146/annurev.arplant.55.031903.141655
38. Kochian L.V., Piñeros M.A., Liu J., Magalhaes J.V. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annual Review of Plant Biology 2015; 66(1):571- 598. DOI: 10.1146/annurev-arplant-043014-114822
39. Koroban N.V., Kudryavtseva A.V., Krasnov G.S., Sad ritdi no va A.F., Fedorova M.S., Snezhkina A.V. et al. The role of microRNA in abiotic stress response in plants. Molecular Biology. 2016;50(3):387-394. [in Russian] DOI: 10.7868/S0026898416020105
40. Kuznetsov V.V. General resistance systems and transduction of a stressor sigbak during plant adaptation to abiotic factors (Obshchiye sistemy ustoychivosti i transduktsiya stressornogo signala pri adaptatsii rasteniy k abioticheskim faktoram. Vestnik Nizhegorodskogo universiteta = Bulletin of Nizhny Novgorod University. 2001;16:65-69. [in Russian]
41. Labrou N.E., Papageorgiou A.C., Pavli O., Flemetakis E. Plant GSTome: structure and functional role in xenome network and plant stress response. Current Opinion in Biotechnology. 2015;32:186-194. DOI: 10.1016/j.copbio.2014.12.024
42. Lawrence G.B., Fernandez I.J., Richter D.D., Ross D.S., Hazlett P.W., Bailey S.W. et al. Measuring environmental change in forest ecosystems by repeated soil sampling: a North American perspective. Journal of Environmental Quality. 2013;42(3):623-639. DOI: 10.2134/jeq2012.0378
43. Lima J.C., Arenhart R.A., Margis-Pinheiro M., Margis R. Alu mi num triggers broad changes in microRNA expression in rice roots. Genetics and Molecular Research. 2011;10(4):2817-2832. DOI: 10.4238/2011.November.10.4
44. Ma J.F., Ryan P.R., Delhaize E. Aluminum tolerance in plants and the complexing role of organic acids. Trends in Plant Science. 2001;6(6):273-278. DOI: org/10.1016/S1360-1385(01)01961-6
45. Melnikova N.V., Kudryavtseva A.V., Bolsheva N.L., Speran skaya A.S., Krinitsina A.A., Rozhmina T.A. et al. High-throughput sequencing methods for molecular evaluation of response of flax genotypes to stressful environmental factors. Agrarian Re porter of South-East. 2016;1-2:63-64. [in Russian].
46. Mendoza-Soto A.B, Naya L., Leija A., Hernández G. Responses of symbiotic nitrogen-fixing common bean to aluminum toxicity and delineation of nodule responsive microRNAs. Frontiers in Plant Science. 2015;6:587. DOI: org/10.3389/fpls.2015.00587
47. Mockaitis K., Estelle M. Auxin receptors and plant development: a new signaling paradigm. Annual Review of Cell and Developmental Biology 2008;24(1):55-80. DOI: org/10.1146/annurev.cellbio.23.090506.123214
48. Montgomery T.A., Howell M.D., Cuperus J.T., Li D., Hansen J.E., Alexander A.L. et al. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell. 2008;133(1):128-141. DOI: 10.1016/j.cell.2008.02.033
49. Nag A., King S., Jack T. miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(52):22534-22539. DOI: org/10.1073/pnas.0908718106
50. Nahar K., Hasanuzzaman M., Suzuki T., Fujita M. Polyaminesinduced aluminum tolerance in mung bean: A study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology. 2017;26(1):58-73. DOI: 10.1007/s10646-016-1740-9
51. Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science. 2006;312(5772):436-439. DOI: 10.1126/science.1126088
52. Nebolsin A.N., Sychev V.G. Ecological and economic bases and recommendations for liming adapted to specific soil conditions. (Ekologo-ekonomicheskiye osnovy i rekomendatsii po izvestkovaniyu, adaptirovannye k konkretnym pochvennym usloviyam). Moscow; St. Petersburg: TsINAO; 2000. [in Russian].
53. Nekrasov R.V., Ovcharenko M.M., Akanova N.I. Agroeco logical foundation of chemical amelioration of soils. Amelioration of Soils. Zemledelie. 2019;4:3-7. [in Russian]. DOI: 10.24411/0044-3913-201910401
54. Omidbakhshfard M.A., Proost S., Fujikura U., MuellerRoeber B. Growth-regulating factors (GRFs): A small transcription factor family with important functions in plant biology. Molecular Plant. 2015;8(7):998-1010. DOI: 10.1016/j.molp.2015.01.013
55. Palatnik J.F., Allen E., Wu X., Schommer C., Schwab R., Carrington J.C. et al. Control of leaf morphogenesis by microRNAs. Nature. 2003;425(6955):257-263. DOI 10.1038/nature01958
56. Panda S.K., Baluška F., Matsumoto H. Aluminum stress signaling in plants. Plant Signaling and Behavior. 2009;4(7):592-597. DOI: org/10.4161/psb.4.7.8903
57. Panda S.K., Matsumoto H. Changes in antioxidant gene expression and induction of oxidative stress in pea (Pisum sativum L.) under Al stress. BioMetals. 2010;23(4):753-762. DOI: 10.1007/s10534-010-9342-0
58. Poland J. Breeding-assisted genomics. Current Opinion in Plant Biology. 2015;24:119-124. DOI: 10.1016/j.pbi.2015.02.009
59. Ponomareva L.V., Drichko V.F., Tsvetkova N.P., Kud ryavtsev D.V. Content of mobile aluminum and soil acidity on the background of cultivation of aluminum-tolerant bacteria for the purpose of rising of plants resistance. Agricultural Biology. 2010;45(1):104-109. [in Russian].
60. Promenasheva T.E., Kolesnichenko L.S., Kozlova N.M. Role oxidative stress and glutathione system in the pathogenesis of nonalcoholic fatty liver disease. Acta Biomedica Scientifica (East Siberian Biomedical Journal). 2014;(5):80- 83. [in Russian].
61. Pukhal’skaya N.V. Debatable problems of aluminum toxicity Agrokhimiya = Agrochemistry. 2005;8:70-82. [in Russian].
62. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B., Bartel D.P. MicroRNAs in plants. Genes and Development. 2002;16(13):1616-1626. DOI: 10.1101/gad.1004402
63. Richard K.D., Schott E.J., Sharma Y.K., Davis K.R., Gardner R.C. Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology. 1998;116(1):409- 418. DOI: 10.1104/pp.116.1.409
64. Sade H., Meriga B., Surapu V., Gadi J., Sunita M.S., Suravajhala P. et al. Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils. BioMetals. 2016;29:187-210. DOI: 10.1007/s10534-016-9910-z
65. Sampson M., Clarkson D.T., Davies D. DNA synthesis in aluminum treated roots of barley. Science. 1965;148:1476-1472.
66. Schommer C., Debernardi J.M., Bresso E.G., Rodriguez R.E., Palatnik J.F. Repression of cell proliferation by miR319- regulated TCP4. Molecular Plant. 2014;7(10):1533-1544. DOI: 10.1093/mp/ssu084
67. Sharma S.S., Dietz K.J. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany. 2006;57(4):711-726. DOI: 10.1093/jxb/erj073
68. Shilnikov I.A., Ermolaev S.A., Akanova N.I. Calcium balance and dynamics of acidity of arable soils under liming conditions. (Balans kaltsiya i dinamika kislotnosti pakhotnykh pochv v usloviyakh izvestkovaniya). Moscow; 2006. [in Russian].
69. Sorokina O.Yu., Nechushkin S.M. Role of calcium and magnesium cations and soil acidity in the yielding capacity of fiber flax. Agrokhimiya = Agrochemistry. 2005;10:13-17. [in Russian]
70. Srivalli S., Khanna-Chopra R. Role of glutathione in abiotic stress tolerance. In: N.A. Khan, S. Singh, S. Umar (eds). Sulfur Assimilation and Abiotic Stress in Plants. Berlin; Heidelberg: Springer-Verlag; 2008. p.207-225. DOI: 10.1007/978-3-540-76326-0
71. Sunkar R. MicroRNAs with macro-effects on plant stress responses. Seminars in Cell and Developmental Biology. 2010;21(8):805-811. DOI: 10.1016/j.semcdb.2010.04.001
72. Taylor G.J. The physiology of aluminum tolerance in higher plants Communications in Soil Science and Plant Analysis. 1988;19(7-12):1179-1194.
73. Udovenko G.V. Physiological basis of plant breeding (Fiziologicheskiye osnovy selektsii rasteniy). In: G.V. Udovenko, V.S. Shevelukha (eds). Theoretical Basis of Plant Breeding. Vol. 2. Pt 2. St. Petersburg: VIR; 1995. [in Russian].
74. Wang Z., Hobson N., Galindo L., Zhu S., Shi D., McDill J. et al. The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. The Plant Journal. 2012;72(3):461-473. DOI: 10.1111/j.1365-313X.2012.05093.x
75. Wojcik A.M., Gaj M.D. miR393 contributes to the embryogenic transition induced in vitro in Arabidopsis via the modification of the tissue sensitivity to auxin treatment. Planta. 2016;244(1):231-243. DOI: org/10.1007/s00425-016-2505-7
76. Yakovleva O.V. Phytotoxicity of aluminum ions. Proceedings on Applied Botany, Genetics and Breeding. 2018;179(3):315- 331. [in Russian]. DOI: 10.30901/2227-8834-2018-3-315-331
77. Yang L.T., Qi Y.P., Jiang H.X., Chen L.S. Roles of organic acid anion secretion in aluminium tolerance of higher plants. BioMed Research International. 2013;2013:173682. DOI: 10.1155/2013/173682
78. Zelenin A.V. Plant genome (Genom rasteniy). Vestnik Rossiyskoy akademii nauk = Bulleting of the Russian Academy of Sciences. 2003;73(9):797-806. [in Russian]
79. Zeng Q.Y., Yang C.Y., Ma Q.B., Li X.P., Dong W.W., Nian H. Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biology. 2012;12:182. DOI: 10.1186/1471-2229-12-182
80. Zhang J., Wei J., Li D., Kong X., Rengel Z., Chen L. et al. The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. Frontiers in Plant Science. 2017;8:1757. DOI: 10.3389/fpls.2017.01757
81. Zhao X., Chen Q., Wang Y., Shen Z., Shen W., Xu X. Hydrogenrich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis. Ecotoxicology and Environmental Safety. 2017;144:369-379. DOI: 10.1016/j.ecoenv.2017.06.045
82. Zheng S.J. Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Annals of Botany, 2010;106(1):183-184. DOI: 10.1093/aob/mcq134
83. Zheng S.J., Yang J.L., He Y.F., Yu X.H., Zhang L., You J.F. et al. Immobilization of aluminum with phosphorus in roots is associated with high aluminum resistance in buckwheat. Plant Physiology. 2005;138(1):297-303. DOI: 10.1104/pp.105.059667
84. Zhuchenko A.A. Adaptive system of plant breeding (ecogenetic fundamentals). Vol. 2 (Adaptivnaya sistema selektsii rasteniy [ekologo-geneticheskiye osnovy]. T. 2). Moscow: RUDN; 2001. [in Russian]
Review
For citations:
Kishlyan N.V., Melnikova N.V., Rozhmina T.A. The mechanisms of fiber flax adaptation to high soil acidity (a review). Proceedings on applied botany, genetics and breeding. 2020;181(4):205-212. (In Russ.) https://doi.org/10.30901/2227-8834-2020-4-205-212