Skip to main content

Potential role of D-myo-inositol-3-phosphate synthase and 14-3-3 genes in the crosstalk between Zea mays and Rhizophagus intraradices under drought stress

Abstract

Arbuscular mycorrhizal (AM) symbiosis is known to stimulate plant drought tolerance. However, the mechanisms underlying the synergistic responses of the symbiotic partners to drought stress are largely unknown. A split-root experiment was designed to investigate the molecular interactions between a host plant and an AM fungus (AMF) under drought stress. In the two-compartment cultivation system, an entire or only a half root system of a maize plant was inoculated with an AMF, Rhizophagus intraradices, in the presence of localized or systemic drought treatment. Plant physiological parameters including growth, water status, and phosphorus concentration, and the expression of drought tolerance-related genes in both roots and R. intraradices were recorded. Although mycorrhizal inoculation in either one or both compartments systemically decreased abscisic acid (ABA) content in the whole root system subjected to systemic or local drought stress, we observed local and/or systemic AM effects on root physiological traits and the expression of functional genes in both roots and R. intraradices. Interestingly, the simultaneous increase in the expression of plant genes encoding D-myo-inositol-3-phosphate synthase (IPS) and 14-3-3-like protein GF14 (14-3GF), which were responsible for ABA signal transduction, was found to be involved in the activation of 14-3-3 protein and aquaporins (GintAQPF1 and GintAQPF2) in R. intraradices. These findings suggest that coexpression of IPS and 14-3GF is responsible for the crosstalk between maize and R. intraradices under drought stress, and potentially induces the synergistic actions of the symbiotic partners in enhancing plant drought tolerance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Aroca R, Vernieri P, Ruiz-Lozano JM (2008) Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Biol 59:2029–2041

    CAS  Google Scholar 

  • Atzmon N, Salomon E, Reuveni O, Riov J (1994) Lateral root formation in pine seedlings. II. The role of assimilates. Trees-Struct Funct 8:273–277

    Article  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Bárzana G, Aroca R, Ruiz-Lozano JM (2015) Localized and non-localized effects of arbuscular mycorrhizal symbiosis on accumulation of osmolytes and aquaporins and on antioxidant systems in maize plants subjected to total or partial root drying. Plant Cell Environ 38:1613–1627

    Article  PubMed  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Camp ROD, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg É, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  Google Scholar 

  • Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314–325

    CAS  Article  PubMed  Google Scholar 

  • De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439

    Article  PubMed  Google Scholar 

  • Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotechnol 23:547–552

    CAS  Article  PubMed  Google Scholar 

  • Dewar RC (1993) A root-shoot partitioning model based on carbon-nitrogen-water interactions and Munch phloem flow. Funct Ecol 7:356–368

    Article  Google Scholar 

  • Dickson RE (1991) Assimilate distribution and storage. In: Raghavendra AS (ed) Physiology of trees. Wiley, New York, pp 51–85

    Google Scholar 

  • Doerner P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11:536–540

    CAS  Article  PubMed  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F-tests. Biometrics 11:1–42

    Article  Google Scholar 

  • Estrada-Luna AA, Davies FT (2003) Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. J Plant Physiol 160:1073–1083

    CAS  Article  PubMed  Google Scholar 

  • Fujii H, Zhu JK (2012) Osmotic stress signaling via protein kinases. Cell Mol Life Sci 69:3165–3173

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • García Garrido JM, León Morcillo RJ, Martín Rodríguez JA, Ocampo Bote JA (2010) Variations in the mycorrhization characteristics in roots of wild-type and ABA-deficient tomato are accompanied by specific transcriptomic alterations. MPMI 23:651–664

    Article  Google Scholar 

  • Gónzalez-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140

    Article  PubMed  Google Scholar 

  • Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:346–355

    Article  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in tomato arbuscular mycorrhiza. New Phytol 175:554–564

    CAS  Article  PubMed  Google Scholar 

  • Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479

    CAS  Article  PubMed  Google Scholar 

  • Jeschke WD, Hartung W (2000) Root-shoot interactions in mineral nutrition. Plant Soil 226:57–69

    CAS  Article  Google Scholar 

  • Ji XM, Dong BD, Shiran B, Talbot MJ, Edlington JE, Hughes T, White RG, Gubler F, Dolferus R (2011) Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiol 156:647–662

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jia JJ, Fu JJ, Zheng J, Zhou X, Huai JL, Wang JH, Wang M, Zhang Y, Chen XP, Zhang JP, Zhao JF, Su Z, Lv YP, Wang GY (2006) Annotation and expression profile analysis of 2073 full-length cDNAs from stress-induced maize (Zea mays L.) seedlings. Plant J 48:710–727

    CAS  Article  PubMed  Google Scholar 

  • Joshi-Saha A, Valon C, Leung J (2011) A brand new START: abscisic acid perception and transduction in the guard cell. Sci Signal 4:re4

    Article  PubMed  Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schnidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712

    CAS  Article  PubMed  Google Scholar 

  • Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD (2013) First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 197:617–630

    CAS  Article  PubMed  Google Scholar 

  • Li T, Lin G, Zhang X, Chen YL, Zhang SB, Chen BD (2014) Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 24:595–602

    Article  PubMed  Google Scholar 

  • Libault M, Brechenmacher L, Cheng JL, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641–650

    CAS  Article  PubMed  Google Scholar 

  • Lin K, Limpens E, Zhang ZH, Ivanov S, Saunders DGO, Mu DS, Pang EL, Cao HF, Cha HH, Lin T, Zhou Q, Shang Y, Li Y, Sharma T, van Velzen R, de Ruijter N, Aanen DK, Win J, Kamoun S, Bisseling T, Huang SW (2014) Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10:e1004078

    Article  PubMed  PubMed Central  Google Scholar 

  • Munns R, Sharp RE (1993) Involvement of abscisic acid in controlling plant growth in soils of low water potential. Aust J Plant Physiol 20:425–437

    CAS  Article  Google Scholar 

  • Murphy AM, Otto B, Brearley CA, Carr JP, Hanke DE (2008) A role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Plant J 56:638–652

    CAS  Article  PubMed  Google Scholar 

  • Neumann E, Schmid B, Rӧmheld V, George E (2009) Extraradical development and contribution to plant performance of an arbuscular mycorrhizal symbiosis exposed to complete or partial rootzone drying. Mycorrhiza 20:13–23

    Article  PubMed  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458

    CAS  Article  PubMed  Google Scholar 

  • Peuke AD, Jeschke WD, Hartung W (1994) The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long distance transport of abscisic acid depending on nitrogen nutrition and salt stress. J Exp Bot 45:741–747

    CAS  Article  Google Scholar 

  • Peuke AD, Jeschke WD, Hartung W (2002) Flows of elements, ions and abscisic acid in Ricinus communis and site of nitrate reduction under potassium limitation. J Exp Bot 53:241–250

    CAS  Article  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29:45

    Article  Google Scholar 

  • Porcel R, Azcon R, Ruiz-Lozano JM (2004) Evaluation of the role of genes encoding for △1-pyrroline-5-carboxylate synthetase (P5CS) during drought stress in arbuscular mycorrhizal Glycine max and Lactuca sativa plants. Physiol Mol Plant P 65:211–221

    CAS  Article  Google Scholar 

  • Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2006a) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404

    CAS  Article  PubMed  Google Scholar 

  • Porcel R, Aroca R, Cano C, Bago A, Ruiz-Lozano JM (2006b) Identification of a gene from the arbuscular mycorrhizal fungus Glomus intraradices encoding for a 14-3-3 protein that is up-regulated by drought stress during the AM symbiosis. Microb Ecol 52:575–582

    Article  PubMed  Google Scholar 

  • Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 50:1031–1039

    CAS  Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcon R (1997) Effect of calcium application on the tolerance of mycorrhizal lettuce plants to polyethylene glycol-induced water stress. Symbiosis 23:9–22

    Google Scholar 

  • Ruiz-Lozano JM, del Mar Alguacil M, Barzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70:565–579

    CAS  Article  PubMed  Google Scholar 

  • Ruíz-Sánchez M, Armada E, Muňoz Y, de Salamone IEG, Aroca R, Ruíz-Lozano JM, Azcón R (2011) Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 168:1031–1037

    Article  PubMed  Google Scholar 

  • Schoonheim PJ, Sinnige MP, Casaretto JA, Veiga H, Bunney TD, Quatrano RS, de Boer AH (2007) 14-3-3 adaptor proteins are intermediates in ABA signal transduction during barley seed germination. Plant J 49:289–301

    CAS  Article  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    CAS  Article  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  Article  PubMed  Google Scholar 

  • Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    Google Scholar 

  • Stevenson-Paulik J, Bastidas RJ, Chiou ST, Frye RA, York JD (2005) Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci U S A 102:12612–12617

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the National Natural Science Foundation of China (41371264, 41401281) and the Chinese Academy of Sciences (XDB15030102).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baodong Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 30 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, T., Sun, Y., Ruan, Y. et al. Potential role of D-myo-inositol-3-phosphate synthase and 14-3-3 genes in the crosstalk between Zea mays and Rhizophagus intraradices under drought stress. Mycorrhiza 26, 879–893 (2016). https://doi.org/10.1007/s00572-016-0723-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-016-0723-2

Keywords

  • Abscisic acid
  • Arbuscular mycorrhizal fungus
  • Drought tolerance
  • Gene regulation
  • Maize
  • Rhizophagus intraradices