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Comparative transcriptome analysis reveals positive effects of arbuscular mycorrhizal fungi inoculation on photosynthesis and high-pH tolerance in blueberry seedlings

  • Lu Yang
  • Qing-Qing Li
  • Yan Yang
  • Qiang Chen
  • Xuan Gao
  • Jia-Xin XiaoEmail author
Original Article
  • 61 Downloads
Part of the following topical collections:
  1. Mycorrhiza

Key message

Our results based on transcriptome data and physiological alterations give an account for enhancing high-pH tolerance in blueberry seedlings with AMF inoculation.

Abstract

To understand the responses occurring in leaves of arbuscular mycorrhizal fungi (AMF)-inoculated plants under high-pH stress, we combined physiological analyses with leaf transcriptome profiles of AMF-inoculated and non-inoculated blueberry (Vaccinium corymbosum) cultivar “O’Neal” under optimal-pH (pH 4.2) and high-pH (pH 6.2) conditions. Comparative transcriptome analysis revealed 250 differentially expressed genes (DEGs) in AMF-inoculated plants when compared with non-inoculated plants under high-pH stress. These DEGs were involved in 37 metabolic pathways, such as photosynthesis, hormone metabolism, carbohydrate metabolism, amino acid metabolism, stress response, signal transduction, and antioxidation. Physiological analyses revealed that AMF-inoculated plants presented lower respiration and higher photosynthesis efficiency under high-pH stress, along with accumulation of photosystem II reaction center PsbP family protein, enhancement of amino acids content, and stronger secondary metabolites biosynthesis ability, when compared with non-inoculated plants. These results provide new insights into a probable mechanism of protection of photosynthesis and enhancement of high-pH tolerance in blueberry seedlings with AMF inoculation.

Keywords

Mycorrhiza Vaccinium corymbosum Blueberry High-pH stress Transcriptome Photosynthesis 

Notes

Acknowledgements

This work was supported by the Provincial Natural Science Research Program of Higher Education of Anhui province (KJ2016SD24 and KJ2019A0484) and the Doctoral Program Foundation (2018) of Anhui Normal University (751863).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (XLS 28 kb)
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Supplementary material 3 (XLSX 33 kb)
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Supplementary material 4 (DOCX 23 kb)

References

  1. Arriagada C, Manquel D, Cornejo P, Soto J, Sampedro I, Ocampo J (2012) Effects of the co-inoculation with saprobe and mycorrhizal fungi on Vaccinium corymbosum growth and some soil enzymatic activities. J Soil Sci Plant Nutr 12(2):287–298.  https://doi.org/10.4067/S0718-95162012000200008 CrossRefGoogle Scholar
  2. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113.  https://doi.org/10.1146/annurev.arplant.59.032607.092759 CrossRefPubMedGoogle Scholar
  3. Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MÁ, Valdez-Ortiz Á, López-Meyer M (2016) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-Seq analysis. Plant Mol Biol Rep 34(1):89–102.  https://doi.org/10.1007/s11105-015-0903-9 CrossRefGoogle Scholar
  4. Chen YY, Hu CY, Xiao JX (2014) Effects of arbuscular mycorrhizal inoculation on the growth, zinc distribution and photosynthesis of two citrus cultivars grown in low-zinc soil. Trees 28:1427–1436.  https://doi.org/10.1007/s00468-014-1046-6 CrossRefGoogle Scholar
  5. Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Exp Bot 75:25–35.  https://doi.org/10.1016/j.envexpbot.2011.08.012 CrossRefGoogle Scholar
  6. Druge U, Schonbeck F (1993) Effect of vesicular-arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L.) in relation to cytokinin levels. J Plant Physiol 141:40–48.  https://doi.org/10.1016/S0176-1617(11)80849-7 CrossRefGoogle Scholar
  7. Gao LX, Li S, Mo AQ, Liu FM, Chen Y, Zhou ZZ, Zeng RS (2012) Effects of inoculation of arbuscular mycorrhizal fungi on growth of rabbiteye blueberry (Vaccinium ashei Reade) in south China. Ecol Environ Sci 21(8):1413–1417Google Scholar
  8. Gao X, Zhao S, Xu Q-L, Xiao J-X (2016) Transcriptome responses of grafted Citrus sinensis plants to inoculation with the arbuscular mycorrhizal fungus Glomus versiforme. Trees 30:1073–1082.  https://doi.org/10.1007/s00468-015-1345-6 CrossRefGoogle Scholar
  9. Gerlach N, Schmitz J, Polatajko A, Schlüter U, Fahnenstich H, Witt S, Fernie AR, Uroic K, Scholz U, Sonnewald U, Bucher M (2015) An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. Plant Cell Environ 38(8):1591–1612.  https://doi.org/10.1111/pce.12508 CrossRefPubMedGoogle Scholar
  10. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512.  https://doi.org/10.1038/nprot.2013.084 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60(9):2465–2480.  https://doi.org/10.1093/jxb/erp144 CrossRefPubMedGoogle Scholar
  12. Kogel KH, Voll LM, Schäfer P, Jansen C, Wu Y, Langen G, Imani J, Hofmann J, Schmiedl A, Sonnewald S, Wettstein DV, Cook RJ, Sonnewald U (2010) Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific variances. Proc Natl Acad Sci USA 107(14):6198–6203.  https://doi.org/10.1073/pnas.1001945107 CrossRefPubMedGoogle Scholar
  13. Laparre J, Malbreil M, Letisse F, Portais JC, Roux C, Bécard G, Puech-Pagès V (2014) Combining metabolomics and gene expression analysis reveals that propionyl-and butyryl-carnitines are involved in late stages of arbuscular mycorrhizal symbiosis. Mol Plant 7(3):554–566.  https://doi.org/10.1093/mp/sst136 CrossRefPubMedGoogle Scholar
  14. Li QQ, Lu SS, Zhang H, Yang Y, Xiao JX (2017) Physiological response to different soil pH values between Vaccinium bracteatum and Vaccinium ashei. J Zhejiang Uni 43(4):469–475.  https://doi.org/10.3785/j.issn.1008-9209.2016.08.281 CrossRefGoogle Scholar
  15. Ouzounidou G, Skiada V, Papadopoulou KK, Stamatis N, Kavvadias V, Eleftheriadis E, Gaitis F (2015) Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical composition of chia (Salvia hispanica L.) leaves. Braz J Bot 38(3):487–495.  https://doi.org/10.1007/s40415-015-0166-6 CrossRefGoogle Scholar
  16. Payá-Milans M, Nunez GH, Olmstead JW, Rinehart TA, Staton M (2017) Regulation of gene expression in roots of the pH-sensitive Vaccinium corymbosum and the pH-tolerant Vaccinium arboretum in response to near neutral pH stress using RNA-Seq. BMC Genom 18:580.  https://doi.org/10.1186/s12864-017-3967-0 CrossRefGoogle Scholar
  17. Phillips JM, Hayman DS (1970) Improve procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161.  https://doi.org/10.1016/s0007-1536(70)80110-3 CrossRefGoogle Scholar
  18. Rivero J, Gamir J, Aroca R, Pozo MJ, Flors V (2015) Metabolic transition in mycorrhizal tomato roots. Front Microbiol 6:598.  https://doi.org/10.3389/fmicb.2015.00598 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Schweiger R, Baier MC, Müller C (2014) Arbuscular mycorrhiza-induced shifts in foliar metabolism and photosynthesis mirror the developmental stage of the symbiosis and are only partly driven by improved phosphate uptake. Mol Plant Microbe In 27(12):1403–1412.  https://doi.org/10.1094/MPMI-05-14-0126-R CrossRefGoogle Scholar
  20. Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430.  https://doi.org/10.1007/s00572-010-0353-z CrossRefPubMedGoogle Scholar
  21. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Amsterdam.  https://doi.org/10.1016/b978-0-12-370526-6.x5001-6 CrossRefGoogle Scholar
  22. Souza LA, Camargos LS, Schiavinato MA, Andrade SAL (2014) Mycorrhization alters foliar soluble amino acid composition and influences tolerance to Pb in Calopogonium mucunoides. Theor Exp Plant Physiol 26:211–216.  https://doi.org/10.1007/s40626-014-0019-x CrossRefGoogle Scholar
  23. Vega AR, Garciga M, Rodríguez A, Prat L, Mella J (2009) Blueberries mycorrhizal symbiosis outside of the boundaries of natural dispersion for ericaceous plants in Chile. Acta Hort 810:665–671.  https://doi.org/10.17660/ActaHortic.2009.810.88 CrossRefGoogle Scholar
  24. Wang XK (2006) Experimental principle and technique for plant physiology and biochemistry. Higher Education Press, Beijing, pp 134–136Google Scholar
  25. Wang M, Wilde J, Baldwin LT, Groten K (2018) Nicotiana attenuata’ s capacity to interact with arbuscular mycorrhiza alters its competitive ability and elicits major changes in the leaf transcriptome: AMF-induced systemic changes in genes and metabolites. J Integr Plant Biol 60(3):242–261.  https://doi.org/10.1111/jipb.12609 CrossRefPubMedGoogle Scholar
  26. Williamson JG, Mejia L, Ferguson B, Miller P, Haman DZ (2015) Seasonal water use of southern highbush blueberry plants in a subtropical climate. HortTechnology 25(2):185–191CrossRefGoogle Scholar
  27. Wu W-H (2012) Plant physiology. Science Press, Beijing, pp 137–154Google Scholar
  28. Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425.  https://doi.org/10.1016/j.jplph.2005.04.024 CrossRefPubMedGoogle Scholar
  29. Xu CX, Ma YP, Chen H (2014) Technique of grafting with Wufanshu(Vaccinium bracteatum Thunb.) and the effects on blueberry plant growth and development, fruit yield and quality. Sci Hort 176:290–296.  https://doi.org/10.1016/j.scienta.2014.07.021 CrossRefGoogle Scholar
  30. Yano K, Takaki M (2005) Mycorrhizal alleviation of acid soil stress in the sweet potato (Ipomoea batatas). Soil Biol Biochem 37:1569–1572.  https://doi.org/10.1016/j.soilbio.2005.01.010 CrossRefGoogle Scholar
  31. Zhao X-L, Zhang J-X, Chen C-L, Yang J-Z, Zhu H-Y, Liu M, Lv F-B (2014) Deep sequencing-based comparative transcriptional profiles of Cymbidium hybridum roots in response to mycorrhizal and non-mycorrhizal fungi. BMC Genom 15:747.  https://doi.org/10.1186/1471-2164-15-747 CrossRefGoogle Scholar
  32. Zhu XC, Song FB, Xu HW (2010) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137.  https://doi.org/10.1007/s11104-009-0239-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lu Yang
    • 1
  • Qing-Qing Li
    • 1
  • Yan Yang
    • 1
  • Qiang Chen
    • 1
  • Xuan Gao
    • 1
  • Jia-Xin Xiao
    • 1
    Email author
  1. 1.Key Laboratory for the Conservation and Utilization of Important Biological Resources, Anhui Province, College of Life SciencesAnhui Normal UniversityWuhuChina

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