Plant hormones have become appropriate candidates for driving functional plant mycorrhization programs, including the processes that regulate the formation of arbuscules in arbuscular mycorrhizal (AM) symbiosis. Here, we examine the role played by ABA/GA interactions regulating the formation of AM in tomato. We report differences in ABA and GA metabolism between control and mycorrhizal roots. Active synthesis and catabolism of ABA occur in AM roots. GAs level increases as a consequence of a symbiosis-induced mechanism that requires functional arbuscules which in turn is dependent on a functional ABA pathway. A negative interaction in their metabolism has been demonstrated. ABA attenuates GA-biosynthetic and increases GA-catabolic gene expression leading to a reduction in bioactive GAs. Vice versa, GA activated ABA catabolism mainly in mycorrhizal roots. The negative impact of GA3 on arbuscule abundance in wild-type plants is partially offset by treatment with ABA and the application of a GA biosynthesis inhibitor rescued the arbuscule abundance in the ABA-deficient sitiens mutant. These findings, coupled with the evidence that ABA application leads to reduce bioactive GA1, support the hypothesis that ABA could act modifying bioactive GA level to regulate AM. Taken together, our results suggest that these hormones perform essential functions and antagonize each other by oppositely regulating AM formation in tomato roots.

Department of Soil Microbiology and Symbiotic Systems Estación Experimental del Zaidín Consejo Superior de Investigaciones Científicas Granada Spain

Institut für Botanik Technische Universität Dresden Dresden Germany

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany Academy of Sciences of the Czech Republic v v i Palacký University Olomouc Czech Republic

Zobrazit více v PubMed

Achard P., Cheng H., Grauwe L., Decat J., Schoutteten H., Moritz T., et al. (2006). Integration of plant responses to environmentally activated phytohormonal signals. PubMed DOI

Balestrini R., Gómez-Ariza J., Lanfranco L., Bonfante P. (2007). Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculared cells. PubMed DOI

Bassel G. W., Mullen R. T., Bewley J. D. (2008). Procera is a putative DELLA mutant in tomato ( PubMed DOI

Bonfante P., Genre A. (2010). Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. PubMed DOI

Brown R. G. S., Kawaide H., Yang Y. Y., Kamiya Y. (1997). Daminozide and prohexadione have similar modes of action as inhibitors of the late stages of gibberellin metabolism. DOI

Chabot C., Bécard G., Piché Y. (1992). Life cycle of DOI

Charpentier M., Sun J., Wen J., Mysore K. S., Oldroyd G. (2014). ABA promotion of arbuscular mycorrhizal colonization requires a component of the PP2A protein phosphatase complex. PubMed DOI PMC

Chitarra W., Pagliarani C. H., Maserti B., Lumini E., Siciliano I., Cascone P., et al. (2016). Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. PubMed DOI PMC

Cosme M., Ramireddy E., Franken P., Schmülling T., Wurst S. (2016). Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis. PubMed DOI PMC

El Ghachtouli N., Martin-Tanguy J., Paynot M., Gianinazzi S. (1996). First report of the inhibition of arbuscular mycorrhizal infection of PubMed DOI

Etemadi M., Gutjahr C., Couzigou J.-M., Zouine M., Lauressergues D., Timmers A., et al. (2014). Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. PubMed DOI PMC

Fiorilli V., Catoni M., Miozzi L., Novero M., Accotto G. P., Lanfranco L. (2009). Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. PubMed DOI

Floss D., Levy J., Lévesque-Tremblay V., Pumplin N., Harrison M. (2013). DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. PubMed DOI PMC

Foo E., Rossi J. J., Jones W. T., Reid J. B. (2013). Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. PubMed DOI PMC

García-Garrido J. M., León-Morcillo R. J., Martín-Rodríguez J. A., Ocampo-Bote J. A. (2010). Variations in the mycorrhization characteristics in roots of wild-type and ABA-deficient tomato are accompanied by specific transcriptomic alterations. PubMed DOI

Gonai T., Kawahara S., Tougou M., Satoh S., Hashiba T., Hirai N., et al. (2004). Abscisic acid in the thermoinhibition of lettuce seed germination and enhancement of its catabolism by gibberellin. PubMed DOI

Gutjahr C. (2014). Phytohormone signaling in arbuscular mycorrhiza development. PubMed DOI

Hedden P., Thomas G. (2012). Gibberellin biosynthesis and its regulation. PubMed DOI

Herrera-Medina M. J., Steinkellner S., Vierheilig H., Ocampo Bote J. A., García-Garrido J. M. (2007). Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. PubMed DOI

Hewitt E. J. (1966).

Hradecká V., Novák O., Havlíček L., Strnad M. (2007). Immunoaffinity chromatography of abscisic acid combined with electrospray liquid chromatography-mass spectrometry. PubMed DOI

Kang S. M., Kim J. T., Hamayun M., Hwang I. C., Khan A. L., Kim Y. H., et al. (2010). Influence of prohexadione-calcium on growth and gibberellins content of Chinese cabbage grown in alpine region of South Korea. DOI

Kim H. Y., Lee I. J., Hamayun M., Kim J. T., Won J. G., Hwang I. C., et al. (2007). Effect of prohexadione calcium on growth components and endogenous gibberellins contents of rice ( DOI

Kim Y. H., Khan A. L., Hamayun M., Kim J. T., Lee J. H., Hwang I. C., et al. (2010). Effects of prohexadione calcium on growth and gibberellins contents of DOI

Kucera B., Cohn M. A., Leubner-Metzger G. (2005). Plant hormone interactions during seed dormancy release and germination. DOI

Kushiro T., Okamoto M., Nakabayashi K., Yamagishi K., Kitamura S., Asami T., et al. (2004). The PubMed DOI PMC

Lee K. H., Piao H. L., Kim H. Y., Choi S. M., Jiang F., Hartung W., et al. (2006). Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. PubMed DOI

Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. PubMed DOI

López-Ráez J. A., Kohlen W., Charnikhova T., Mulder P., Undas A. K., Sergeant M. J., et al. (2010). Does abscisic acid affect strigolactone biosynthesis? PubMed DOI

Ludwig-Müller J. (2010). “Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi,” in

Mahouachi J., Gómez-Cadenas A., Primo-Millo E., Talon M. (2005). Antagonistic changes between abscisic acid and gibberellins in citrus fruits subjected to a series of different water conditions. DOI

Martín-Rodríguez J. A., León-Morcillo R., Vierheilig H., Ocampo Bote J. A., Ludwig-Müllerm J., García-Garrido J. M., et al. (2010). Mycorrhization of the PubMed DOI

Martín-Rodríguez J. A., León-Morcillo R. J., Vierheilig H., Ocampo-Bote J. A., Ludwig-Müller J., García-Garrido J. M. (2011). Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. PubMed DOI

Martín-Rodríguez J. A., Ocampo J. A., Molinero-Rosales N., Tarkowská D., Ruíz-Rivero O., García-Garrido J. M. (2015). Role of gibberellins during arbuscular mycorrhizal formation in tomato: new insights revealed by endogenous quantification and genetic analysis of their metabolism in mycorrhizal roots. PubMed DOI

Oh E., Yamaguchi S., Hu J. H., Yusuke J., Jung B., Paik I., et al. (2007). PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in PubMed DOI PMC

Phillips J. M., Hayman D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. DOI

Pimprikar P., Carbonnel S., Paries M., Katzer K., Klingl V., Bohmer M. J., et al. (2016). A CCaMK-CYCLOPS-DELLA complex activates transciption of RAM1 to regulate arbuscule branching. PubMed DOI

Pozo M. J., López-Ráez J. A., Azcón C., García-Garrido J. M. (2015). Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. PubMed DOI

Rittenberg D., Foster G. L. (1940). New procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids.

Rodríguez-Gacio M., Matilla-Vázquez M. A., Matilla A. J. (2009). Seed dormancy and ABA signaling. PubMed DOI PMC

Ruiz-Lozano J. M., Aroca R., Zamarreño A. M., Molina S., Andreo-Jiménez B., Porcel R., et al. (2016). Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. PubMed DOI

Schüßler A., Walker C. (2010).

Seo M., Hanada A., Kuwahara A., Endo A., Okamoto M., Yamauchi Y., et al. (2006). Regulation of hormone metabolism in PubMed DOI

Shaul-Keinan O., Gadkar V., Ginzberg I., Grünzweig J. M., Chet I., Elad Y., et al. (2002). Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with PubMed DOI

Shu K., Chen Q., Wu Y., Liu R., Zhang H., Wang P., et al. (2016). ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. PubMed DOI

Silverstone A., Jung H.-S., Dill A., Kawaide H., Kamiya Y., Sun T. (2001). Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in PubMed DOI PMC

Smith S. E., Read D. J. (2008).

Taylor I. B., Linforth R. S. T., Al Naieb R. J., Bowman W. R., Marples B. A. (1988). The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. DOI

Trouvelot A., Kough J. L., Gianinazzi-Pearson V. (1986). “Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de methods d’estimation ayant une signification fonctionelle,” in

Turečková V., Novák O., Strnad M. (2009). Profiling ABA metabolites in PubMed DOI

Urbanová T., Tarkowská D., Novák O., Hedden P., Strnad M. (2013). Analysis of gibberellins as free acids by ultra-performance liquid chromatography–tandem mass spectrometry. PubMed DOI

Van Tuinen A., Peters A. H. L. J., Kendrick R. E., Zeevaart J. A. D., Koornneef M. (1999). Characterisation of the procera mutant of tomato and the interaction of gibberellins with end-of-day far-red light treatments. DOI

Weiss D., Ori N. (2007). Mechanisms of cross talk between gibberellin and other hormones. PubMed DOI PMC

White C. N., Proebsting W. M., Hedden P., Rivin C. J. (2000). Gibberellins and seed development in maize. PubMed DOI PMC

Yu N., Luo D., Zhang X., Liu J., Wang W., Jin Y., et al. (2014). A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. PubMed DOI PMC

Zentella R., Zhang Z. L., Park M., Thomas S. G., Endo A., Murase K., et al. (2007). Global analysis of DELLA direct targets in early gibberellin signaling in PubMed DOI PMC

The SlDLK2 receptor, involved in the control of arbuscular mycorrhizal symbiosis, regulates hormonal balance in roots

A dual regulatory role for the arbuscular mycorrhizal master regulator RAM1 in tomato

Zaxinone synthase controls arbuscular mycorrhizal colonization level in rice