The effect of arbuscular mycorrhiza on gene expression of sweet family in Medicago lupulina under conditions of high available phosphorus level

Abstract

BACKGROUND: According to modern concepts, the SWEET family may be the only family of plant sugar transporters that includes genes specifically expressed during the formation and development of plant symbiosis with fungi of arbuscular mycorrhiza. The data on the key genetic markers of the development of effective arbuscular mycorrhiza symbiosis can contribute an active development of organic agriculture in various conditions of phosphorus availability in the soil.

AIM: to evaluate the effect of arbuscular mycorrhiza on the expression of SWEET genes in M. lupulina L. during key stages of host plant development (stages of leaves rosette, stooling initiation, stooling, lateral branching initiation, lateral branching and flowering).

MATERIALS AND METHODS: The study was performed using a highly efficient plant-microbial system “Medicago lupulina + Rhizophagus irregularis” grown under conditions with a high content of available phosphorus in the substrate.

RESULTS: Under condition of high phosphorus level in the substrate it was shown for the first time the MlSWEET1b and MlSWEET3c genes in M. lupulina leaves were characterized by specific expression during mycorrhization.

CONCLUSIONS: MlSWEET1b and MlSWEET3c and their orthologs can be considered as marker genes of effective symbiosis development, as a tool of biotechnology to increase agricultural productivity with using biostimulants based on arbuscular mycorrhiza fungi.

Keywords

arbuscular mycorrhiza / Medicago lupulina / Rhizophagus irregularis / effective symbiosis / development / markers of symbiotic effiiency

References

[1] Smith SE, Read DJ. Mycorrhizal symbiosis. Academic press; 2010.

[2] Smith S.E., Read D.J. Mycorrhizal symbiosis. Academic press, 2010.

[3] Schüßler A. Glomeromycota species list. Available from: http://www.amf-phylogeny.com

[4] Schüßler A. Glomeromycota species list. Режим доступа: http://www.amf-phylogeny.com

[5] Chen L-Q, Hou B-H, Lalonde S, et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010;468(7323):527–532. doi: 10.1038/nature09606

[6] Chen L.-Q., Hou B.-H., Lalonde S., et al. Sugar transporters for intercellular exchange and nutrition of pathogens // Nature. 2010. Vol. 468, N 7323. P. 527–532. doi: 10.1038/nature09606

[7] Kryukov AA, Gorbunova AO, Kudriashova TR, et al. Sugar transporters of the SWEET family and their role in arbuscular mycorrhiza. Vavilov Journal of Genetics and Breeding. 2021;25(7):754–760. doi: 10.18699/VJ21.086 EDN: PNTAAU

[8] Крюков А.А., Горбунова А.О., Кудряшова Т.Р., и др. Транспортеры сахаров семейства SWEET и их роль в арбускулярной микоризе // Вавиловский журнал генетики и селекции. 2021. Т. 25, № 7. С. 754–760. doi: 10.18699/VJ21.086 EDN: PNTAAU

[9] Chen L-Q, Cheung L-S, Feng L, et al. Transport of sugars. Annu Rev Biochem. 2015;84(1):865–894. doi: 10.1146/annurev-biochem-060614-033904

[10] Chen L.-Q., Cheung L.-S., Feng L., et al. Transport of sugars // Annu Rev Biochem. 2015. Vol. 84, N 1. P. 865–894. doi: 10.1146/annurev-biochem-060614-033904

[11] Chen L-Q, Qu X-Q, Hou B-H, et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012;335(6065):207–211. doi: 10.1126/science.1213351

[12] Chen L.-Q., Qu X.-Q., Hou B.-H., et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport // Science. 2012. Vol. 335, N 6065. P. 207–211. doi: 10.1126/science.1213351

[13] Feng C-Y, Han J-X, Han X-X, Jiang J. Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene. 2015;573(2):261–272. doi: 10.1016/j.gene.2015.07.055

[14] Feng C.-Y., Han J.-X., Han X.-X., Jiang J. Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato // Gene. 2015. Vol. 573, N 2. P. 261–272. doi: 10.1016/j.gene.2015.07.055

[15] Hu B, Wu H, Huang W, et al. SWEET gene family in Medicago truncatula: genome-wide identification, expression and substrate specificity analysis. Plants. 2019;8(9):338. doi: 10.3390/plants8090338

[16] Hu B., Wu H., Huang W., et al. SWEET gene family in Medicago truncatula: genome-wide identification, expression and substrate specificity analysis // Plants. 2019. Vol. 8, N 9. ID 338. doi: 10.3390/plants8090338

[17] Kanno Y, Oikawa T, Chiba Y, et al. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat Commun. 2016;7(1):13245. doi: 10.1038/ncomms13245

[18] Kanno Y., Oikawa T., Chiba Y., et al. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes // Nat Commun. 2016. Vol. 7, N 1. ID 13245. doi: 10.1038/ncomms13245

[19] Manck-Götzenberger J, Requena N. Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci. 2016;7:487. doi: 10.3389/fpls.2016.00487

[20] Manck-Götzenberger J., Requena N. Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family // Front Plant Sci. 2016. Vol. 7. ID 487. doi: 10.3389/fpls.2016.00487

[21] Yurkov AP, Jacobi LM, Gapeeva NE, et al. Development of arbuscular mycorrhiza in highly responsive and mycotrophic host plant–black medick (Medicago lupulina L.). Russian Journal of Developmental Biology. 2015;46:263–275. doi: 10.1134/S1062360415050082

[22] Yurkov A.P., Jacobi L.M., Gapeeva N.E., et al. Development of arbuscular mycorrhiza in highly responsive and mycotrophic host plant–black medick (Medicago lupulina L.) // Russian Journal of Developmental Biology. 2015. Vol. 46. P. 263–275. doi: 10.1134/S1062360415050082

[23] Yurkov AP, Afonin AM, Kryukov AA, et al. The effects of Rhizophagus irregularis inoculation on transcriptome of Medicago lupulina leaves at early vegetative and flowering stages of plant development. Plants. 2023;12(20):3580. doi: 10.3390/plants12203580

[24] Yurkov A.P., Afonin A.M., Kryukov A.A., et al. The effects of Rhizophagus irregularis inoculation on transcriptome of Medicago lupulina leaves at early vegetative and flowering stages of plant development // Plants. 2023. Vol. 12, N 20. ID 3580. doi: 10.3390/plants12203580

[25] Kryukov AA, Gorbunova AO, Kudriashova TR, et al. SWEET transporters of Medicago lupulina in the arbuscular-mycorrhizal system in the presence of medium level of available phosphorus.Vavilov Journal of Genetics and Breeding. 2023;27(3):189–196. doi: 10.18699/VJGB-23-25 EDN: NHSLXC

[26] Крюков А.А., Горбунова А.О., Кудряшова Т.Р., и др. SWEET транспортеры Medicagolupulina в арбускулярно-микоризной системе в условиях среднего уровня доступного фосфора // Вавиловский журнал генетики и селекции. 2023. Т. 27, № 3. С. 189–196. doi: 10.18699/VJGB-23-25 EDN: NHSLXC

[27] Kryukov AA, Yurkov AP. Optimization procedures for molecular-genetic identification of arbuscular mycorrhizal fungi in symbiotic phase on the example of two closely kindred strains. Mycology and phytopathology. 2018;52(1):38–48. EDN: YQLCGE

[28] Крюков А.А., Юрков А.П. Оптимизация процедуры молекулярно-генетической идентификации грибов арбускулярной микоризы в симбиотическую фазу на примере двух близкородственных штаммов // Микология и фитопатология. 2018. Т. 52, № 1. С. 38–48. EDN: YQLCGE

[29] Yurkov AP, Puzanskiy RK, Avdeeva GS, et al. Mycorrhiza-induced alterations in metabolome of Medicago lupulina leaves during symbiosis development. Plants. 2021;10(11):2506. doi: 10.3390/plants10112506

[30] Yurkov A.P., Puzanskiy R.K., Avdeeva G.S., et al. Mycorrhiza-induced alterations in metabolome of Medicago lupulina leaves during symbiosis development // Plants. 2021. Vol. 10, N 11. ID 2506. doi: 10.3390/plants10112506

[31] Yurkov A, Kryukov A, Gorbunova A, et al. AM-induced alteration in the expression of genes, encoding phosphorus transporters and enzymes of carbohydrate metabolism in Medicago lupulina. Plants. 2020;9(4):486. doi: 10.3390/plants9040486

[32] Yurkov A., Kryukov A., Gorbunova A., et al. AM-induced alteration in the expression of genes, encoding phosphorus transporters and enzymes of carbohydrate metabolism in Medicago lupulina // Plants. 2020. Vol. 9, N 4. ID 486. doi: 10.3390/plants9040486

[33] Yurkov AP, Puzanskiy RK, Kryukov AA, et al. The role of Medicago lupulina interaction with Rhizophagus irregularis in the determination of root metabolome at early stages of am symbiosis. Plants. 2022;11(18):2338. doi: 10.3390/plants11182338

[34] Yurkov A.P., Puzanskiy R.K., Kryukov A.A., et al. The role of Medicago lupulina interaction with Rhizophagus irregularis in the determination of root metabolome at early stages of am symbiosis // Plants. 2022. Vol. 11, N 18. ID 2338. doi: 10.3390/plants11182338

[35] Klechkovsky VM, Petersburg AV. Agrochemistry. Moscow: Kolos; 1967. 584 p. (In Russ.)

[36] Клечковский В.М., Петербургский А.В. Агрохимия. Москва: Колос, 1967. 584 с.

[37] Sokolov AV. Agrochemical methods of soil research. Moscow: Nauka; 1975. 656 p. (In Russ.)

[38] Соколов А.В. Агрохимические методы исследования почв. Москва: Наука, 1975. 656 с.

[39] MacRae E. Extraction of plant RNA. In: Hilario E, Mackay J, editors. Protocols for nucleic acid analysis by nonradioactive probes. Methods in molecular biology. Vol. 353. Humana Press; 2007. P. 15–24. doi: 10.1385/1-59745-229-7:15

[40] MacRae E. Extraction of plant RNA. В кн.: Protocols for nucleic acid analysis by nonradioactive probes. Methods in molecular biology. Vol. 353 / E. Hilario, J. Mackay, editors. Humana Press, 2007. P. 15–24. doi: 10.1385/1-59745-229-7:15

[41] Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc. 1970;55(1): 158–161 IN16–IN18. doi: 10.1016/S0007-1536(70)80110-3

[42] Phillips J.M., Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection // Trans Br Mycol Soc. 1970. Vol. 55, N 1. P. 158–161 IN16–IN18. doi: 10.1016/S0007-1536(70)80110-3

[43] Trouvelot A, Kough JL, Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S, editors. Physiological and genetical aspects of mycorrhizae. Paris: INRA-Press; 1986. P. 217–221.

[44] Trouvelot A., Kough J.L., Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes ayant une signification fonctionnelle. В кн.: Physiological and genetical aspects of mycorrhizae / V. Gianinazzi-Pearson, S. Gianinazzi, editors. Paris: INRA-Press, 1986. P. 217–221.

[45] Certificate of registration of the computer program No. 2010612112/ 02.12.2016. Vorobyev NI, Yurkov AP, Provorov NA. Program for calculation of indicators of mycorrhization of plant roots. Moscow: Rospatent; 2016. (In Russ.)

[46] Свидетельство о регистрации программы для ЭВМ № 2010612112/ 02.12.2016. Воробьев Н.И., Юрков А.П., Проворов Н.А. Программа для расчета показателей микоризации корней растений. Москва: Роспатент, 2016.

[47] Kaur S, Campbell BJ, Suseela V. Root metabolome of plant–arbuscular mycorrhizal symbiosis mirrors the mutualistic or parasitic mycorrhizal phenotype. New Phytol. 2022;234(2):672–687. doi: 10.1111/nph.17994

[48] Kaur S., Campbell B.J., Suseela V. Root metabolome of plant–arbuscular mycorrhizal symbiosis mirrors the mutualistic or parasitic mycorrhizal phenotype // New Phytol. 2022. Vol. 234, N 2. P. 672–687. doi: 10.1111/nph.17994

[49] An J, Zeng T, Ji C, et al. A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytol. 2019;224(1):396–408. doi: 408 10.1111/nph.15975

[50] An J., Zeng T., Ji C., et al. A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis // New Phytol. 2019. Vol. 224, N 1. P. 396–408. doi: 408 10.1111/nph.15975

[51] Tamayo E, Figueira-Galán D, Manck-Götzenberger J, Requena N. Over expression of the potato monosaccharide transporter StSWEET7a promotes root colonization by symbiotic and pathogenic fungi by increasing root sink strength. Front Plant Sci. 2022;13:837231. doi: 10.3389/fpls.2022.837231

[52] Tamayo E., Figueira-Galán D., Manck-Götzenberger J., Requena N. Overexpression of the potato monosaccharide transporter StSWEET7a promotes root colonization by symbiotic and pathogenic fungi by increasing root sink strength // Front Plant Sci. 2022. Vol. 13. ID 837231. doi: 10.3389/fpls.2022.837231

[53] Pu C, Yang G, Li P, et al. Arbuscular mycorrhiza alters the nutritional requirements in Salvia miltiorrhiza and low nitrogen enhances the mycorrhizal efficiency. Sci Rep. 2022;12(1):19633. doi: 10.1038/s41598-022-17121-2

[54] Pu C., Yang G., Li P., et al. Arbuscular mycorrhiza alters the nutritional requirements in Salvia miltiorrhiza and low nitrogen enhances the mycorrhizal efficiency // Sci Rep. 2022. Vol. 12, N 1. ID 19633. doi: 10.1038/s41598-022-17121-2

[55] Calonne-Salmon M, Plouznikoff K, Declerck S. The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 increases the phosphorus uptake and biomass of Medicago truncatula, a benzo[a]pyrene-tolerant plant species. Mycorrhiza. 2018;28(8): 761–771. doi: 10.1007/s00572-018-0861-9

[56] Calonne-Salmon M., Plouznikoff K., Declerck S. The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 increases the phosphorus uptake and biomass of Medicago truncatula, a benzo[a]pyrene-tolerant plant species // Mycorrhiza. 2018. Vol. 28, N 8. P. 761–771. doi: 10.1007/s00572-018-0861-9

[57] Doidy J, Vidal U, Lemoine R. Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum. PLoS One. 2019;14(9):e0223173. doi: 10.1371/journal.pone.0223173

[58] Doidy J., Vidal U., Lemoine R. Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum // PLoS One. 2019. Vol. 14, N 9. ID e0223173. doi: 10.1371/journal.pone.0223173

[59] Bui VC, Franken P. Acclimatization of Rhizophagus irregularis enhances Zn tolerance of the fungus and the mycorrhizal plant partner. Front Microbiol. 2018;9:3156. doi: 10.3389/fmicb.2018.03156

[60] Bui V.C., Franken P. Acclimatization of Rhizophagus irregularis enhances Zn tolerance of the fungus and the mycorrhizal plant partner // Front Microbiol. 2018. Vol. 9. ID 3156. doi: 10.3389/fmicb.2018.03156

[61] Schweiger R, Baier MC, Persicke M, Müller C. High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nat Commun. 2014;5(1):3886. doi: 10.1038/ncomms4886

[62] Schweiger R., Baier M.C., Persicke M., Müller C. High specificity in plant leaf metabolic responses to arbuscular mycorrhiza // Nat Commun. 2014. Vol. 5, N 1. ID 3886. doi: 10.1038/ncomms4886

[63] Cope K, Kafle A, Yakha JK, et al. Physiological and transcriptomic response of Medicago truncatula to colonization by high-or low-benefit arbuscular mycorrhizal fungi. Mycorrhiza. 2022;32(3):281–303. doi: 10.1007/s00572-022-01077-2

[64] Cope K., Kafle A., Yakha J.K., et al. Physiological and transcriptomic response of Medicago truncatula to colonization by high-or low-benefit arbuscular mycorrhizal fungi // Mycorrhiza. 2022. Vol. 32, N 3. P. 281–303. doi: 10.1007/s00572-022-01077-2

[65] Chandran D. Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB life. 2015;67(7):461–471. doi: 10.1002/iub.1394

[66] Chandran D. Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance // IUBMB life. 2015. Vol. 67, N 7. P. 461–471. doi: 10.1002/iub.1394

[67] Ho L-H, Klemens PAW, Neuhaus HE, et al. SlSWEET1a is involved in glucose import to young leaves in tomato plants. J Exp Bot. 2019;70(12):3241–3254. doi: 10.1093/jxb/erz154

[68] Ho L.-H., Klemens P.A.W., Neuhaus H.E., et al. SlSWEET1a is involved in glucose import to young leaves in tomato plants // J Exp Bot. 2019. Vol. 70, N 12. P. 3241–3254. doi: 10.1093/jxb/erz154

[69] Gautam T, Saripalli G, Gahlaut V, et al. Further studies on sugar transporter (SWEET) genes in wheat (Triticum aestivum L.). Mol Biol Rep. 2019;46:2327–2353. doi: 10.1007/s11033-019-04691-0

[70] Gautam T., Saripalli G., Gahlaut V., et al. Further studies on sugar transporter (SWEET) genes in wheat (Triticum aestivum L.) // Mol Biol Rep. 2019. Vol. 46. P. 2327–2353. doi: 10.1007/s11033-019-04691-0

[71] Li M, Xie H, He M, et al. Genome-wide identification and expression analysis of the StSWEET family genes in potato (Solanum tuberosum L.). Genes and Genomics. 2020;42:135–153. doi: 10.1007/s13258-019-00890-y

[72] Li M., Xie H., He M., et al. Genome-wide identification and expression analysis of the StSWEET family genes in potato (Solanum tuberosum L.) // Genes and Genomics. 2020. Vol. 42. P. 135–153. doi: 10.1007/s13258-019-00890-y

[73] Li X, Si W, Qin Q, et al. Deciphering evolutionary dynamics of SWEET genes in diverse plant lineages. Sci Rep. 2018;8(1):13440. doi: 10.1038/s41598-018-31589-x

[74] Li X., Si W., Qin Q., et al. Deciphering evolutionary dynamics of SWEET genes in diverse plant lineages // Sci Rep. 2018. Vol. 8, N 1. ID 13440. doi: 10.1038/s41598-018-31589-x

[75] Sugiyama A, Saida Y, Yoshimizu M, et al. Molecular characterization of LjSWEET3, a sugar transporter in nodules of Lotus japonicas. Plant Cell Physiol. 2017;58(2):298–306. doi: 10.1093/pcp/pcw190

[76] Sugiyama A., Saida Y., Yoshimizu M., et al. Molecular characterization of LjSWEET3, a sugar transporter in nodules of Lotus japonicus // Plant Cell Physiol. 2017. Vol. 58, N 2. P. 298–306. doi: 10.1093/pcp/pcw190

Funding

Russian Science FoundationРоссийский научный фонд(22-16-00064)

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