Advertisement

Impact of arbuscular mycorrhizal fungi (AMF) on gene expression of some cell wall and membrane elements of wheat (Triticum aestivum L.) under water deficit using transcriptome analysis

  • Zahra Moradi Tarnabi
  • Alireza IranbakhshEmail author
  • Iraj Mehregan
  • Rahim Ahmadvand
Research Article
  • 39 Downloads

Abstract

Mycorrhizal symbiotic relationship is one of the most common collaborations between plant roots and the arbuscular mycorrhizal fungi (AMF). The first barrier for establishing this symbiosis is plant cell wall which strongly provides protection against biotic and abiotic stresses. The aim of this study was to investigate the gene expression changes in cell wall of wheat root cv. Chamran after inoculation with AMF, Funneliformis mosseae under two different irrigation regimes. To carry out this investigation, total RNA was extracted from the roots of mycorrhizal and non-mycorrhizal plants, and analyzed using RNA-Seq in an Illumina Next-Seq 500 platform. The results showed that symbiotic association between wheat and AMF and irrigation not only affect transcription profile of the plant growth, but also cell wall and membrane components. Of the 114428 genes expressed in wheat roots, the most differentially expressed genes were related to symbiotic plants under water stress. The most differentially expressed genes were observed in carbohydrate metabolic process, lipid metabolic process, cellulose synthase activity, membrane transports, nitrogen compound metabolic process and chitinase activity related genes. Our results indicated alteration in cell wall and membrane composition due to mycorrhization and irrigation regimes might have a noteworthy effect on the plant tolerance to water deficit.

Keywords

Arbuscular mycorrhizae Plant cell wall RNA-Seq Triticum aestivum Water deficit 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. An J, Sun M, Velzen R, Ji C, Zheng Z, Limpens E, Bisseling T, Deng X, Xiao S, Pan Z (2018) Comparative transcriptome analysis of Poncirus trifoliate identifies a core set of genes involved in arbuscular mycorrhizal symbiosis. J Exp Bot 69(21):5255–5264.  https://doi.org/10.1093/jxb/ery283 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Balestrini R, Bonfante P (2014) Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5:237.  https://doi.org/10.3389/fpls.2014.00237 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524CrossRefGoogle Scholar
  4. Behringer D, Zimmermann H, Ziegenhagen B, Liepelt S (2015) Differential gene expression reveals candidate genes for drought stress response in Abies alba (Pinaceae). PLoS ONE.  https://doi.org/10.1371/journal.pone.0124564 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R, Ruphael Y, Colla G, Terzi V, Lucini L (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Biochem 137:203–212.  https://doi.org/10.1016/j.plaphy CrossRefPubMedGoogle Scholar
  6. Boudart G, Charpentier M, Lafitte C, Martinez Y, Jauneau A, Gaulin E, Esquerré-Tugayé MT, Dumas B (2003) Elicitor activity of a fungal endopolygalacturonase in tobacco requires a functional catalytic site and cell wall localization. Plant Physiol 131(1):93–101.  https://doi.org/10.1104/pp.011585 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491(7426):705–710.  https://doi.org/10.1038/nature11650 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 27(4):1352–1366.  https://doi.org/10.1105/tpc.114.131144 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen X, Song F, Liu F, Tian C, Liu S, Xu H, Zhu X (2014) Effect of different Arbuscular Mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes. Sci World J Article ID 956141, 7.  https://doi.org/10.1155/2014/956141 Google Scholar
  10. Clavijo BJ, Venturini L, Schudoma C, Accinelli GG, Kaithakottil G, Wright J et al (2017) An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res 27:885–896.  https://doi.org/10.1101/gr.217117.116 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Couto M, Lovato P, Wipf D, Dumas-Gaudot E (2013) Proteomic studies of arbuscular mycorrhizal associations. Adv Biol Chem 3:48–58.  https://doi.org/10.4236/abc.2013.31007 CrossRefGoogle Scholar
  12. Dana MM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142(2):722–730.  https://doi.org/10.1104/pp.106.086140 CrossRefPubMedCentralGoogle Scholar
  13. Dong CH, Li C, Yan XH, Huang SM, Huang JY, Wang LJ, Guo RX, Lu GY, Zhang XK, Fang XP, Wei WH (2012) Gene expression profiling of Sinapis alba leaves under drought stress and rewatering growth conditions with Illumina deep sequencing. Mol Biol Rep 39(5):5851–5857.  https://doi.org/10.1007/s11033-011-1395 CrossRefPubMedGoogle Scholar
  14. Essahibi A, Benhiba L, Babram MA, Ghoulam C, Qaddoury A (2018) Influence of arbuscular mycorrhizal fungi on the functional mechanisms associated with drought tolerance in carob (Ceratonia siliqua L.). Trees 32:87–97.  https://doi.org/10.1007/s00468-017-1613-84 CrossRefGoogle Scholar
  15. Garcia K, Chasman D, Roy S, Ané JM (2017) Physiological responses and gene co-expression network of mycorrhizal roots under K + deprivation. Plant Physiol 173:1811–1823CrossRefGoogle Scholar
  16. Gill BS, Appels R, Botha-Oberholster AM, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorák J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T (2004) A workshop report on wheat genome sequencing: international genome research on wheat consortium. Genetics 168(2):1087–1096.  https://doi.org/10.1534/genetics.104.034769 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotusjaponicus. New Phytol 182(1):200–212.  https://doi.org/10.1111/j.1469-8137.2008.02725 CrossRefPubMedGoogle Scholar
  18. Gutjahr C, Sawers RJH, Marti G, Andrés-Hernández L, Yang SY, Casieri L et al (2015) Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proc Natl Acad Sci USA 112:6754–6759.  https://doi.org/10.1073/pnas.1504142112 CrossRefPubMedGoogle Scholar
  19. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K, Molinaro A, Kaku H, Shibuya N (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA 111(3):404–413.  https://doi.org/10.1073/pnas.1312099111 CrossRefGoogle Scholar
  20. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158(1):17–25.  https://doi.org/10.1099/mic.0.052274-0 CrossRefPubMedGoogle Scholar
  21. Hong JJ, Park YS, Bravo A, Bhattarai KK, Daniels DA, Harrison MJ (2012) Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236:851–865.  https://doi.org/10.1007/s00425-012-1677 CrossRefPubMedGoogle Scholar
  22. Houston K, Tucker MR, Chowdhury J, Shirley N, Little A (2016) The plant cell wall: a complex and dynamic structure as revealed by the responses of genes under stress conditions. Front Plant Sci 7:984.  https://doi.org/10.3389/fpls.2016.00984 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ivanov S, Harrison MJ (2018) Accumulation of phosphoinositides in distinct regions of the periarbuscular membrane. New Phytol 221(4):2213–2227.  https://doi.org/10.1111/nph.15553 CrossRefPubMedGoogle Scholar
  24. Ivanov S, Austin J, Berg RH, Harrison MJ (2019) Extensive membrane systems at the host-arbuscular mycorrhizal fungus interface. Nat Plants 5:194–203.  https://doi.org/10.1038/s41477-019-0364-5 CrossRefPubMedGoogle Scholar
  25. Jacott CN, Murray JD, Ridout CJ (2017) Trade-offs in arbuscular mycorrhizal symbiosis: disease resistance, growth responses and perspectives for crop breeding. Agronomy 7(4):75.  https://doi.org/10.3390/agronomy7040075 CrossRefGoogle Scholar
  26. Jayasena AS, Secco D, Bernath-Levin K, Berkowitz O, Whelan J, Mylne JS (2014) Next generation sequencing and de novo transcriptomics to study gene evolution. Plant Methods 10(1):34.  https://doi.org/10.1186/1746-4811-10-34 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kesten C, Menna A, Sánchez-Rodríguez C (2017) Regulation of cellulose synthesis in response to stress. Curr Opin Plant Biol 40:106–113.  https://doi.org/10.1016/j.pbi.2017.08.010 CrossRefPubMedGoogle Scholar
  28. Keunen E, Peshev D, Vangronsveld J, Van Dem Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant, Cell Environ 36:1242–1255.  https://doi.org/10.1111/pce.12061 CrossRefGoogle Scholar
  29. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36.  https://doi.org/10.1186/gb-2013-14-4-r36 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359.  https://doi.org/10.1038/nmeth CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65(3):799–807.  https://doi.org/10.1093/jxb/ert474 CrossRefPubMedGoogle Scholar
  32. Li M, Wang R, Tian H, Gao Y (2018) Transcriptome responses in wheat roots to colonization by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mycorrhiza 28:747.  https://doi.org/10.1007/s00572-018-0868-2 CrossRefPubMedGoogle Scholar
  33. Li J, Meng B, Chai H, Yang X, Song W, Li S, Lu A, Zhang T, Sun W (2019) Arbuscular Mycorrhizal Fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front Plant Sci.  https://doi.org/10.3389/fpls.2019.00499 CrossRefPubMedPubMedCentralGoogle Scholar
  34. López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61(10):2589–2601.  https://doi.org/10.1093/jxb/erq089 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lucas SJ, Akpınar BA, Šimková H, Kubaláková M, Doležel J, Budak H (2014) Next-generation sequencing of flow-sorted wheat chromosome 5D reveals lineage-specific translocations and widespread gene duplications. BMC Genom 15:1080.  https://doi.org/10.1186/1471-2164-15-1080 CrossRefGoogle Scholar
  36. Malinovsky FG, Fangel JU, Willats WG (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178.  https://doi.org/10.3389/fpls.2014.00178 CrossRefPubMedPubMedCentralGoogle Scholar
  37. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115(3):495–501.  https://doi.org/10.1111/j.1469-8137.1990.tb00476.x CrossRefGoogle Scholar
  38. Nanjareddy K, Arthikala MK, Gómez BM, Blanco L, Lara M (2017) Differentially expressed genes in mycorrhized and nodulated roots of common bean are associated with defense, cell wall architecture, N metabolism, and P metabolism. PLoS ONE.  https://doi.org/10.1371/journal.pone.0182328 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nezhadahmadi A, Hossain PZ, Faruq G (2013) Drought tolerance in wheat. Sci World J.  https://doi.org/10.1155/2013/610721 CrossRefGoogle Scholar
  40. Ouledali S, Ennajeh M, Ferrandino A, Khemira H, Schubert A, Secchi F (2019) Influence of arbuscular mycorrhizal fungi inoculation on the control of stomata functioning by abscisic acid (ABA) in drought-stressed olive plants. S Afr J Bot 121:152–158.  https://doi.org/10.1016/j.sajb.2018.10.024 CrossRefGoogle Scholar
  41. Pérez-Tienda J, Corrêa A, Azcón-Aguilar C, Ferrol N (2014) Transcriptional regulation of host NH4 + transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiol Biochem 75:1–8.  https://doi.org/10.1016/j.plaphy.2013.11.029 CrossRefPubMedGoogle Scholar
  42. Rasmussen R (2001) Quantification on the light cycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR, methods and applications. Springer Press, Heidelberg, pp 21–34CrossRefGoogle Scholar
  43. Ren CG, Kong CC, Yan K, Xie ZH (2019) transcriptome analysis reveals the impact of arbuscular mycorrhizal symbiosis on Sesbania cannabina expose to high salinity. Sci Rep 9:2780.  https://doi.org/10.1038/s41598-019-39463-0 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rich MK, Schorderet M, Reinhardt D (2014) The role of the cell wall compartment in mutualistic symbioses of plants. Front Plant Sci 5:238.  https://doi.org/10.3389/fpls.2014.00238 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64(2):204–214.  https://doi.org/10.1111/j.1365-313X.2010.04324 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156(3):1050–1057.  https://doi.org/10.1104/pp.111.174581 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sugimura Y, Saito K (2017) Transcriptional profiling of arbuscular mycorrhizal roots exposed to high levels of phosphate reveals the repression of cell cycle-related genes and secreted protein genes in Rhizophagus irregularis. Mycorrhiza 27(2):139–146.  https://doi.org/10.1007/s00572-016-0735-y CrossRefPubMedGoogle Scholar
  48. Trouvelot S, Héloir MC, Poinssot B, Gauthier A, Paris F, Guillier C, Combier M, Trdá L, Daire X, Adrian M (2014) Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Crop Sci Hortic 5:592.  https://doi.org/10.3389/fpls.2014.00592 CrossRefGoogle Scholar
  49. Vangelisti A, Natali L, Bernardi R, Sbrana C, Turrini A, Hassani-Pak K, Hughes D, Cavallini A, Giovannetti M, Giordani T (2018) Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots. Sci Rep 8(1):4.  https://doi.org/10.1038/s41598-017-18445-0 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wang Y, Yang L, Zheng Z, Grumet R, Loescher W, Zhu JK, Yang P, Hu Y, Chan Z (2013) Transcriptomic and physiological variations of three Arabidopsis ecotypes in response to salt stress. PLoS ONE 8(7):e69036.  https://doi.org/10.1371/journal.pone.0069036 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wang T, McFarlane HE, Persson S (2016) The impact of abiotic factors on cellulose synthesis. J Exp Bot 67(2):543–552.  https://doi.org/10.1093/jxb/erv488 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Wu QS, Rivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87.  https://doi.org/10.1016/j.scienta.2013.09.010 CrossRefGoogle Scholar
  53. Ye L, Zhao X, Bao E, Cao K, Zou Z (2019) Effects of Arbuscular Mycorrhizal Fungi on watermelon growth, elemental uptake, antioxidant, and photosystem II activities and stress-response gene expressions under salinity-alkalinity stresses. Front Plant Sci.  https://doi.org/10.3389/fpls.2019.00863 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhang L, Peng J, Chen TT, Zhao XH, Zhang SP, Liu SD, Dong HL, Feng L, Yu SX (2014) Effect of drought stress on lipid peroxidation and proline content in cotton roots. J Anim Plant Sci 24(6):1729–1736Google Scholar
  55. Zhu Y, Mang HG, Sun Q, Qian J, Hipps A, Hua J (2012) Gene discovery using mutagen-induced polymorphisms and deep sequencing: application to plant disease resistance. Genetics 192(1):139–146.  https://doi.org/10.1534/genetics CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2019

Authors and Affiliations

  • Zahra Moradi Tarnabi
    • 1
  • Alireza Iranbakhsh
    • 1
    Email author
  • Iraj Mehregan
    • 1
  • Rahim Ahmadvand
    • 2
  1. 1.Department of Biology, Science and Research BranchIslamic Azad UniversityTehranIran
  2. 2.Vegetable Research Department, Seed and Plant Improvement InstituteAgricultural Research, Education and Extension OrganizationKarajIran

Personalised recommendations