Abstract
The association between arbuscular mycorrhizal fungi (AMF) and sorghum, the fifth most cultivated cereal in the world and a staple food for many countries, is relevant to improving phosphorus (P) absorption. The importance of root exudation as a signal for the symbiosis has been shown for several species, but a complete understanding of the signaling molecules involved in the mycorrhizal symbiosis signaling pathway has not yet been elucidated. In this context, we investigated the effect of sorgoleone, one of the most studied allelochemicals and a predominant compound of root exudates in sorghum, on AMF colonization and consequently P uptake and plant growth on a sorghum genotype. The sorghum genotype P9401 presents low endogenous sorgoleone content, and when it was inoculated with Rhizophagus clarus together with 5 and 10 µM sorgoleone, mycorrhizal colonization was enhanced. A significant enhancement of mycorrhizal colonization and an increase of P content and biomass were observed when R. clarus was inoculated together with 20 µM sorgoleone. Thus, our results indicate that sorgoleone influences mycorrhizal colonization, but the mechanisms by which it does so still need to be revealed.
References
Abdelhalim T, Jannoura R, Joergensen R (2019) Mycorrhiza response and phosphorus acquisition efficiency of sorghum cultivars differing in strigolactone composition. Plant Soil. https://doi.org/10.1007/s11104-019-03960-y
Aliche E, Screpanti C, De Mesmaeker A et al (2020). Science and application of strigolactones New Phytol. https://doi.org/10.1111/nph.16489
Amballa H (2011) Dependency of sorghum on arbuscular mycorrhizal colonization for growth and development. J Mycol Plant Pathol 41:537–542
Banasiak J, Borghi L, Stec N et al (2020) The Full-Size ABCG Transporter of Medicago truncatula Is Involved in Strigolactone Secretion. Affecting Arbuscular Mycorrhiza, Front. Plant Sci. https://doi.org/10.3389/fpls.2020.00018
Bernardino K, Pastina MM, Menezes C et al (2019) The genetic architecture of phosphorus efficiency in sorghum involves pleiotropic QTL for root morphology and grain yield under low phosphorus availability in the soil. BMC Plant Biol. https://doi.org/10.1186/s12870-019-1689-y
Besserer A, Puech-Pagès V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. https://doi.org/10.1371/journal.pbio.0040226
Borghi L, Liu G, Emonet A et al (2016) The importance of strigolactone transport regulation for symbiotic signaling and shoot branching. Planta. https://doi.org/10.1007/s00425-016-2503-9
Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH et al (2003) Secondary metabolite signalling in host–parasitic plant interactions. Curr Opin Plant Biol. https://doi.org/10.1016/S1369-5266(03)00065-7
Brunetto G, Rosa DJ, Ambrosini VG et al (2019) Use of phosphorus fertilization and mycorrhization as strategies for reducing copper toxicity in young grapevines. SCI HORTIC-AMSTERDAM. https://doi.org/10.1016/j.scienta.2019.01.026
Canarini A, Kaiser C, Merchant A et al (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00157
Chang M, Netzly DH, Butler LG et al (1986) Chemical regulation of the first natural host germination stimulant for Striga asiatica. J Am Chem Soc. https://doi.org/10.1021/ja00284a074
Chiu CH, Paszkowski U (2019) Mechanisms and impact of symbiotic phosphate acquisition. Csh Perspect Biol. https://doi.org/10.1101/cshperspect.a034603
Czarnota MA, Rimando AM, Weston LA (2003) Evaluation of root exudates of seven sorghum accessions. J Chem Ecol. https://doi.org/10.1023/A:1025634402071
Dayan FE, Howell J, Weidenhamer JD (2009) Dynamic root exudation of sorgoleone and its in planta mechanism of action. J Exp Bot. https://doi.org/10.1093/jxb/erp082
Ejeta G, Gobena D, Shimels M et al (2017) Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. PNAS. https://doi.org/10.1073/pnas.1618965114
Embrapa. Centro Nacional de Pesquisa de Solos. Manual de métodos e análise de solo. 2. Ed. Rio de Janeiro, 1997. 212 o. (Embrapa – CNOS. Documento, 1).
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec. https://doi.org/10.1590/S1413-70542011000600001
Gimsing AL, Baelum J, Dayan F et al (2009) Mineralization of the allelochemical sorgoleone in soil. Chemosphere. https://doi.org/10.1016/j.chemosphere.2009.04.048
Hess DE, Ejeta G, Butler LG (1992) Selecting sorghum genotypes expressing a quantitative biosynthetic trait that confers resistance to Striga. Phytochemistry. https://doi.org/10.1016/0031-9422(92)90023-J
Jesudas AP, Kingsley SJ, Ignacimuthu S (2014) Sorgoleone from Sorghum bicolor as a potent bioherbicide. Res J Recent Sci 3:32–36
Johri AK, Oelmüller R, Dua M et al (2015) Fungal association and utilization of phosphate by plants: success, limitations, and future prospects. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00984
Kobae Y, Kameoka H, Sugimura Y et al (2018) Strigolactone biosynthesis genes of rice are required for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcy001
Kobae Y (2019) Dynamic phosphate uptake in arbuscular mycorrhizal roots under field conditions. Front Environ Sci. https://doi.org/10.3389/fenvs.2018.00159
Lanfranco L, Fiorilli V, Gutjahr C (2018) Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytol. https://doi.org/10.1111/nph.15230
Lee E, Eom A (2015) Growth characteristics of Rhizophagus clarus strains and their effects on the growth of host plants. Mycobiology. https://doi.org/10.5941/MYCO.2015.43.4.444
Liu G, Pfeifer J, Francisco RB et al (2018) Changes in the allocation of endogenous strigolactone improve plant biomass production on phosphate-poor soils. New Phytol. https://doi.org/10.1111/nph.14847
MacLean AM, Bravo A, Harrison MJ (2017) Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell. https://doi.org/10.1105/tpc.17.00555
Mohemed N, Charnikhova T, Fradin EF et al (2018) Genetic variation in Sorghum bicolor strigolactones and their role in resistance against Striga hermonthica. J Exp Bot 69(9):2415–2430. https://doi.org/10.1093/jxb/ery041
Nogueira ARA, Souza GB (2005) Manual de laboratórios: solo, água, nutrição vegetal, nutrição animal e alimentos. Embrapa Pecuária Sudeste, São Carlos, p 313
Pan Z, Baerson SR, Wang M et al (2018) A cytochrome P450 CYP71 enzyme expressed in Sorghum bicolor root hair cells participates in the biosynthesis of the benzoquinone allelochemical sorgoleone. New Phytol. https://doi.org/10.1111/nph.15037
Paszkowski U, Jakovleva L, Boller T (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant Journal. https://doi.org/10.1111/j.1365-313X.2006.02785.x
Rich PJ, Ejeta G, Grenier C (2004) Striga resistance in the wild relatives of sorghum. Crop Sci. https://doi.org/10.2135/cropsci2004.2221
Satish K, Gutema Z, Grenier C et al (2012) Molecular tagging and validation of microsatellite markers linked to the low germination stimulant gene (lgs) for Striga resistance in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 124:989–1003. https://doi.org/10.1007/s00122-011-1763-9
Sarr PS, Ando Y, Nakamura S et al (2020) Sorgoleone release from sorghum roots shapes the composition of nitrifying populations, total bacteria, and archaea and determines the level of nitrification. Biol Fertil Soils 56:145–166. https://doi.org/10.1007/s00374-019-01405-3
Schlemper TR, Leite MFA, Lucheta, AR, et al. (2017) Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fix096
Tibugari H, Chiduza C, Mashingaidze AB et al (2018) Quantification of sorgoleone in sorghum accessions from eight southern African countries. S Afr J Plant and Soil. https://doi.org/10.1080/02571862.2018.1469794
Vergara C, Araújo KEC, Schultz N et al (2019) Plant-mycorrhizal fungi interaction and response to inoculation with different growth-promoting fungi. Pesq Agropec Bras. https://doi.org/10.1590/s1678-3921.pab2019.v54.25140
Wen Z, Li H, Shen Q et al (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol. https://doi.org/10.1111/nph.15833
Yoneyama K, Arakawa R, Ishimoto K et al (2015) Difference in Striga-susceptibility is reflected in strigolactone secretion profile, but not in compatibility and host preference in arbuscular mycorrhizal symbiosis in two maize cultivars. New Phytol. https://doi.org/10.1111/nph.13375
Yoneyama K, Xie X, Kisugi T et al (2013) Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta. https://doi.org/10.1007/s00425-013-1943-8
Funding
This work was supported by Empresa Brasileira de Pesquisa Agropecuária – Embrapa (Grant No 12.14.10.003.00.00). IFO is a recipient of a research fellowship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Capes.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
de Oliveira, I.F., Simeone, M.L.F., de Guimarães, C.C. et al. Sorgoleone concentration influences mycorrhizal colonization in sorghum. Mycorrhiza 31, 259–264 (2021). https://doi.org/10.1007/s00572-020-01006-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-020-01006-1