Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants

Journal of Plant Physiology

Volumn 170, Issue 1, 2013, Pages 47-55

  Aroca, Ricardo ^a   Ruiz Lozano, Juan Manuel ^a   Zamarreño, ángel María ^b   Paz, José Antonio ^a   García Mina, José María ^b   Pozo, María José ^a   López Ráez, Juan Antonio ^a  

^a CSIC   (Spain)

^b R and D TAI Roullier Group   (Spain)

Author keywords

Abscisic acid; Arbuscular mycorrhiza; Lettuce; Salt stress; Strigolactones

Indexed keywords

ABSCISIC ACID; LACTONE; SODIUM CHLORIDE;

ARTICLE; BIOMASS; DRUG EFFECT; EVAPOTRANSPIRATION; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GLOMEROMYCOTA; GROWTH, DEVELOPMENT AND AGING; LETTUCE; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT ROOT; PLANT SEED; SALINITY; SYMBIOSIS; TIME;

ABSCISIC ACID; BIOMASS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GLOMEROMYCOTA; LACTONES; LETTUCE; MYCORRHIZAE; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT ROOTS; PLANT TRANSPIRATION; SALINITY; SEEDS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TIME FACTORS;

ARBUSCULAR; FUNGI; LACTUCA;

EID: 84872379795     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2012.08.020     Document Type: Article

References (61)

1. Al-Karaki G.N. Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 2000, 10:51-54.
2. Aliasgharzadeh N., Saleh Rastin N., Towfighi H., Alizadeh A. Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz Plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 2001, 11:119-122.
3. Aroca R., Vernieri P., Ruiz-Lozano J.M. Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. J Exp Bot 2008, 59:2029-2041.
4. Bacaicoa E., Zamarreño A.M., Leménager D., Baigorri R., García-Mina J.M. Relationship between the hormonal balance and the regulation of iron deficiency stress responses in cucumber (Cucumis sativus L.) plants. J Am Soc Hort Sci 2009, 134:589-601.
5. Bouwmeester H.J., Matusova R., Zhongkui S., Beale M.H. Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 2003, 6:358-364.
6. Bouwmeester H.J., Roux C., Lopez-Raez J.A., Bécard G. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 2007, 12:224-230.
7. Cadenas E. Biochemistry of oxygen toxicity. Annu Rev Biochem 1989, 58:79-110.
8. Christmann A., Moes D., Himmelbach A., Yang Y., Tang Y., Grill E. Integration of abscisic acid signalling into plant responses. Plant Biol 2006, 8:314-325.
9. Cuartero J., Bolarín M.C., Asíns M.J., Moreno V. Increasing salt tolerance in the tomato. J Exp Bot 2006, 57:1045-1058.
10. Duan X., Neuman D.S., Reiber J.M., Green C.D., Saxton A.M., Augé R.M. Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought. J Exp Bot 1996, 47:1541-1550.
11. Duncan D.B. Multiple range and multiple F-tests. Biometrics 1955, 11:1-42.
12. Estrada Luna A.A., Davies F.T. 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 2003, 160:1073-1083.
13. Evelin H, Giri B, Kapoor R. Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 2012, in press, doi:10.1007/s00572-012-0449-8.
14. Evelin H., Kapoor R., Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 2009, 104:1263-1280.
15. Fan L., Dalpé Y., Fang C., Dubé C., Khanizadeh S. Influence of arbuscular mycorrhizae on biomass and root morphology of selected strawberry cultivars under salt stress. Botany 2011, 89:397-403.
16. Feng G., Zhang F.S., Li X.L., Tian C.Y., Tang C., Rengel Z. Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 2002, 12:185-190.
17. Fernández-Aparicio M., García-Garrido J.M., Ocampo J.A., Rubiales D. Colonisation of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 2010, 50:262-268.
18. García-Garrido J.M., Lendzemo V., Castellanos-Morales V., Steinkellner S., Vierheilig H. Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 2009, 19:449-459.
19. Germ M., Kreft I., Osvald J. Influence of UV-B exclusion and selenium treatment on photochemical efficiency of photosystem II, yield and respiratory potential in pumpkins (Cucurbita pepo L.). Plant Physiol Biochem 2005, 43:445-448.
20. Giovannetti M., Mosse B. Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 1980, 84:489-500.
21. Giri B., Kapoor R., Mukerji K.G. Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertility Soils 2003, 38:170-175.
22. Gómez-Roldán V., Fermas S., Brewer P.B., Puech-Pagés V., Dun E.A., Pillot J.P., et al. Strigolactone inhibition of shoot branching. Nature 2008, 455:189-194.
23. Hause B., Mrosk C., Isayenkov S., Strack D. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 2007, 68:101-110.
24. Jahromi F., Aroca R., Porcel R., Ruiz-Lozano J.M. Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial Ecol 2008, 55:45-53.
25. Juniper S., Abbott L. Vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 1993, 4:45-58.
26. Juniper S., Abbott L.K. Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 2006, 16:371-379.
27. Kapulnik Y., Delaux P.M., Resnick N., Mayzlish-Gati E., Wininger S., Bhattacharya C., et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 2011, 233:209-216.
28. Kay R., Chan A., Daly M., McPherson J. Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science 1987, 236:1299-1302.
29. Kohlen W., Charnikhova T., Lammers M., Pollina T., Tóth P., Haider I., Pozo M.J., de Maagd R.A., Ruyter-Spira C., Bouwmeester H.J., López-Ráez J.A. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 2012, 196:535-547.
30. Kumar A., Sharma S., Mishra S. Influence of arbuscular mycorrhizal (AM) fungi and salinity on seedling growth, solute accumulation, and mycorrhizal dependency of Jatropha curcas L. J Plant Growth Regul 2010, 29:297-306.
31. t method. Methods 2001, 25:402-408.
32. Loggini B., Scartazza A., Brugnoli E., Navari-Izzo F. Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 1999, 119:1091-1099.
33. López-Ráez J.A., Charnikhova T., Fernández I., Bouwmeester H., Pozo M.J. Arbuscular mycorhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 2011, 168:294-297.
34. López-Ráez J.A., Charnikhova T., Gómez-Roldán V., Matusova R., Kohlen W., De Vos R., et al. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 2008, 178:863-874.
35. López-Ráez J.A., Kohlen W., Charnikhova T., Mulder P., Undas A.K., Sergeant M.J., et al. Does abscisic acid affect strigolactone biosynthesis?. New Phytol 2010, 187:343-354.
36. López-Ráez J.A., Pozo M.J., García-Garrido J.M. Strigolactones: a cry for help in the rhizosphere. Botany 2011, 89:513-522.
37. Matusova R., Rani K., Verstappen F.W.A., Franssen M.C.R., Beale M.H., Bouwmeester H.J. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp are derived from the carotenoid pathway. Plant Physiol 2005, 139:920-934.
38. Ohmiya A. Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 2009, 26:351-358.
39. Oxborough K., Baker N.R. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components - calculation of qP and Fv'/Fm' without measuring Fo'. Photosynth Res 1997, 54:135-142.
40. Parker C. Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 2009, 65:453-459.
41. Phillips J.M., Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 1970, 55:158-161.
42. Porcel R., Aroca R., Ruiz-Lozano J.M. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sust Dev 2012, 32:181-200.
43. Pozo M.J., Azcón-Aguilar C. Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 2007, 10:393-398.
44. Raaijmakers J.M., Paulitz T.C., Steinberg C., Alabouvette C., Moenne-Loccoz Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 2009, 321:341-361.
45. Raghavendra A.S., Gonugunta V.K., Christmann A., Grill E. ABA perception and signalling. Trends Plant Sci 2010, 15:395-401.
46. Redondo-Gómez S., Mateos-Naranjo E., Davy A.J., Fernández-Muñoz F., Castellanos E.M., Luque T., et al. Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Ann Bot 2007, 100:555-563.
47. Redondo-Gómez S., Mateos-Naranjo E., Figueroa M.E., Davy A.J. Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol 2010, 12:79-87.
48. Ruiz-Lozano J.M., Porcel R., Azcon R., Aroca R. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants. New challenges in physiological and molecular studies. J Exp Bot 2012, 63:4033-4044.
49. Ruiz-Sánchez M., Aroca R., Muñoz Y., Polón R., Ruiz-Lozano J.M. The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 2010, 167:862-869.
50. Ruyter-Spira C., Kohlen W., Charnikhova T., van Zeijl A., van Bezouwen L., de Ruijter N., et al. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones?. Plant Physiol 2011, 155:721-734.
51. Sanan-Mishra N., Pham X.H., Sopory S.K., Tuteja N. Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc Natl Acad Sci USA 2005, 102:509-514.
52. Sawada Y., Aoki M., Nakaminami K., Mitsuhashi W., Tatematsu K., Kushiro T., Koshiba T., Kamiya Y., Inoue Y., Nambara E., Toyomasu T. Phytochrome- and gibberellin-mediated regulation of abscisic acid metabolism during germination of photoblastic lettuce seeds. Plant Physiol 2008, 146:1386-1396.
53. Smith F.A., Grace E.J., Smith S.E. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 2009, 182:347-358.
54. Smith S.E., Read D.J. Mycorrhizal symbiosis 2008, Academic Press, London.
55. Stockinger H., Walker C., Schüssler A. 'Glomus intraradices DAOM197198', a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 2009, 183:1176-1187.
56. Taylor I.B., Sonneveld T., Bugg T.D.H., Thompson A.J. Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. J Plant Growth Regul 2005, 24:253-273.
57. Ünlükara A., Cemek B., Karaman S., Erşahin S. Response of lettuce (Lactuca sativa var. crispa) to salinity of irrigation water. N Z J Crop Hort Sci 2008, 36:265-273.
58. Wilde P., Manal A., Stodden M., Sieverding E., Hildebrandt U., Bothe H. Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 2009, 11:1548-1561.
59. Xie X.N., Yoneyama K., Yoneyama K. The strigolactone story. Ann Rev Phytopathol 2010, 48:93-117.
60. Yamato M., Ikeda S., Iwase K. Community of arbuscular mycorrhizal fungi in a coastal vegetation on Okinawa island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza 2008, 18:241-249.
61. Yoneyama K., Xie X., Kusumoto D., Sekimoto H., Sugimoto Y., Takeuchi Y., et al. Nitrogen deficiency as well as phosphorous deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 2007, 227:125-132.