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

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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.

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About the authors

Tatyana R. Kudriashova

All-Russia Research Institute for Agricultural Microbiology; Peter the Great St. Petersburg Polytechnic University

Email: t.kudryashova@arriam.ru
ORCID iD: 0000-0001-5120-7229
SPIN-code: 6716-9431
Russian Federation, Pushkin, Saint Petersburg; Saint Petersburg

Alexey A. Kryukov

All-Russia Research Institute for Agricultural Microbiology

Email: aa.krukov@arriam.ru
ORCID iD: 0000-0002-8715-6723
SPIN-code: 4685-2723

Cand. Sci. (Biology)

Russian Federation, Pushkin, Saint Petersburg

Anastasia O. Gorbunova

All-Russia Research Institute for Agricultural Microbiology

Email: a.gorbunova@arriam.ru
SPIN-code: 3515-6450
Russian Federation, Pushkin, Saint Petersburg

Anastasia I. Gorenkova

All-Russia Research Institute for Agricultural Microbiology; Saint Petersburg State University

Email: nastya.gorenkova.2016@mail.ru
SPIN-code: 3888-9050
Russian Federation, Pushkin, Saint Petersburg; Saint Petersburg

Anastasia Igorevna Kovalchuk

All-Russia Research Institute for Agricultural Microbiology

Email: a.kovalchuk@arriam.ru
SPIN-code: 7051-0285
Russian Federation, Pushkin, Saint Petersburg

Maria F. Shishova

Saint Petersburg State University

Email: mshishova@mail.ru
ORCID iD: 0000-0003-3657-2986
SPIN-code: 7842-7611

Dr. Sci. (Biology), Professor

Russian Federation, Saint Petersburg

Andrey P. Yurkov

All-Russia Research Institute for Agricultural Microbiology

Author for correspondence.
Email: ap.yurkov@arriam.ru
ORCID iD: 0000-0002-1072-5166
SPIN-code: 9909-4280

Cand. Sci. (Biology)

Russian Federation, Pushkin, Saint Petersburg

References

  1. Smith SE, Read DJ. Mycorrhizal symbiosis. Academic press; 2010.
  2. Schüßler A. Glomeromycota species list. Available from: http://www.amf-phylogeny.com
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. Klechkovsky VM, Petersburg AV. Agrochemistry. Moscow: Kolos; 1967. 584 p. (In Russ.)
  19. Sokolov AV. Agrochemical methods of soil research. Moscow: Nauka; 1975. 656 p. (In Russ.)
  20. 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
  21. 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
  22. 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.
  23. 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.)
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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

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2. Fig. 1. Parameters of mycorrhization and AM efficiency (Mycorrhizal Growth Response, MGR) in Medicago lupulina plants at different stages of development during inoculation with Rhizophagus irregularis fungus under condition of high level of available phosphorus in the substrate: a, Mycorrhizal frequency (F, %); b, arbuscule abundance in the root (A, %); c, vesicle abundance in the root (B, %); d, MGR calculated by plant height (%); e, MGR calculated by fresh weight of aboveground parts (%); f, MGR calculated by root fresh weight (%). Significantly different (р <0.05) values of the parameters are marked with different letters.

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3. Fig. 2. Relative transcript levels (normalized values of 2–ΔΔCt) of the main genes of the SWEET family in M. lupulina leaves at a high level of available phosphorus. The average values with the errors of the average values are presented. *Expression levels significantly (p <0.05) differ in the variant with arbuscular mycorrhiza (AM, “sand” column) in comparison with the control without AM fungus inoculation (gray column); ***specific expression levels under conditions of AM fungus inoculation, i.e., the presence of expression in the variant with AM fungus inoculation and in the absence of expression in the control variant without AM fungus inoculation. The expression of the MlSWEET1a and MlSWEET11 was absent, so the data are not presented. © Kryukov A.A. et al., 2023. Permission to use under CC-BY 4.0 license is granted. Borrowed from [13].

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4. Fig. 3. Relative transcript levels (normalized values of 2–ΔΔCt) of the main genes of the SWEET family in M. lupulina roots at a high level of available phosphorus. The average values with the errors of the average values are presented. *Expression levels significantly (p <0,05) differ in the variant with AM (“sand” column) in comparison with the control without AM fungus inoculation (gray column); ***specific expression levels under conditions of AM fungus inoculation. The expression of the MlSWEET1a, MlSWEET7, MlSWEET11 and MlSWEET14 was absent, so these data are not shown in the figure.

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