Strigolactones as mediators between fungi and plants

Anita Kowalczyk, Katarzyna Hrynkiewicz

Abstract


A constantly changing environment is challenging for all organisms on Earth, especially for terrestrial plants, which face several environmental stresses despite their static way of life. In attempts to understand the mechanisms responsible for plant growth and development, scientists have recently focused on a small group of carotenoid derivatives called “strigolactones” (SLs), which are synthesized mostly in the roots in response to a variety of external factors. Strigolactones are compounds that define plant plasticity towards many environmental factors, including the establishment of mycorrhizal symbiosis under nutrient-deficient conditions. As exogenous signals, they can stimulate the branching of arbuscular mycorrhizal fungal (AMF) hyphae and as endogenous signals they adjust a plant architecture, including changes within the roots, allowing host plant and fungi to meet. SLs can also function as signaling molecules that allow colonization and establishment of the later stages of mutualistic symbioses between organisms such as AMF. SLs act on AMF metabolism by stimulating its mitochondrial respiration. Genes encoding enzymes crucial for SL biosynthesis – CCD7 and CCD8 – are also found in gymnosperm genomes, which encourages speculation that strigolactones may also be part of a host-plant and ectomycorrhizal fungi signaling pathway during the establishment of symbiosis. Nevertheless, SLs impact on ectomycorrhiza formation remain unknown. The broad spectrum of SL bioactivity has made these compounds valuable from an industrial perspective. In the future, SLs may be commercialized in plant protection products, biostimulants, or as substances used in genetic engineering to allow the creation of crops capable of growing under disadvantageous conditions.

Keywords


plant–microbial interactions; symbiosis; arbuscular mycorrhizal fungal (AMF); ectomycorrhizal fungi (ECM); pathogenic fungi

Full Text:

PDF

References


Al-Babili S, Bouwmeester HJ. Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol. 2015;66(1):161–186. https://doi.org/10.1146/annurev-arplant-043014-114759

Lopez-Obando M, Ligerot Y, Bonhomme S, Boyer FD, Rameau C. Strigolactone biosynthesis and signaling in plant development. Development. 2015;142(21):3615–3619. https://doi.org/10.1242/dev.120006

Cook CE, Whichard LP, Turner B, Wall ME, Egley GH. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science. 1966;154(3753):1189–1190. https://doi.org/10.1126/science.154.3753.1189

Shen H, Zhu L, Bu QY, Huq E. MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant. 2012;5(3):750–762. https://doi.org/10.1093/mp/sss029

Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA. 2011;108(50):20242–20247. https://doi.org/10.1073/pnas.1111902108

Bu Q, Lv T, Shen H, Luong P, Wang J, Wang Z, et al. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol. 2014;164(1):424–439. https://doi.org/10.1104/pp.113.226837

Vurro M, Prandi C, Baroccio F. Strigolactones: how far is their commercial use for agricultural purposes? Pest Manag Sci. 2016;72(11):2026–2034. https://doi.org/10.1002/ps.4254

Raudaskoski M, Kothe E. Novel findings on the role of signal exchange in arbuscular and ectomycorrhizal symbioses. Mycorrhiza. 2015;25(4):243–252. https://doi.org/10.1007/s00572-014-0607-2

Becard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW. Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbioses. Mol Plant Microbe Interact. 1995;8:252. https://doi.org/10.1094/MPMI-8-0252

Akiyama K, Matsuzaki KI, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005;435(7043):824–827. https://doi.org/10.1038/nature03608

Nagahashi G, Douds DD. Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnology Techniques. 1999;13(12):893–897. https://doi.org/10.1023/A:1008938527757

Tamasloukht M, Séjalon-Delmas N, Kluever A, Jauneau A, Roux C, Bécard G, et al. Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol. 2003;131(3):1468–1478. https://doi.org/10.1104/pp.012898

Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 2006;4(7):1239–1247. https://doi.org/10.1371/journal.pbio.0040226

Besserer A, Becard G, Jauneau A, Roux C, Sejalon-Delmas N. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol. 2008;148(1):402–413. https://doi.org/10.1104/pp.108.121400

Besserer A, Roux C. Role of mitochondria in the response of arbuscular mycorrhizal fungi to strigolactones. Plant Signal Behav. 2009;1(4):75–77. https://doi.org/10.4161/psb.4.1.7419

Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci. 2007;12:224–230. https://doi.org/10.1016/j.tplants.2007.03.009

Nagahashi G, Douds DD. Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi. Mycol Res. 2000;104(12):1453–1464. https://doi.org/10.1017/S0953756200002860

Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, et al. Strigolactone inhibition of shoot branching. Nature. 2008;455(7210):189–194. https://doi.org/10.1038/nature07271

García-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H. Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza. 2009;19(7):449–459. https://doi.org/10.1007/s00572-009-0265-y

Harrison MJ. Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol. 2012;15:691–698. https://doi.org/10.1016/j.pbi.2012.08.010

Kosuta S, Chabaud M, Lougnon G. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 2003;131(3):952–962. https://doi.org/10.1104/pp.011882

Catoira R. Four Genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell. 2000;12(9):1647–1666. https://doi.org/10.1105/tpc.12.9.1647

Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y. Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem. 2000;32(5):589–595. https://doi.org/10.1016/S0038-0717(99)00155-8

Vierheilig H, Maier W, Wyss U, Samson J, Strack D, Piche Y. Cyclohexenone derivative- and phosphate-levels in split-root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. J Plant Physiol. 2000;157(6):593–599. https://doi.org/10.1016/S0176-1617(00)80001-2

Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H. Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol. 2003;157(3):589–595. https://doi.org/10.1046/j.1469-8137.2003.00691.x

Lendzemo VW, Kuyper TW. Effects of arbuscular mycorrhizal fungi on damage by Striga hermonthica on two contrasting cultivars of sorghum, Sorghum bicolor. Agric Ecosyst Environ. 2001;87(1):29–35. https://doi.org/10.1016/S0167-8809(00)00293-0

Harley JL, Smith SE. Mycorrhizal symbiosis. London: Academic Press Inc.; 1983.

Fries N, Serck-Hanssen K, Dimberg LH, Theander O. Abietic acid, and activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (Boletaceae). Exp Mycol. 1987;11(4):360–363. https://doi.org/10.1016/0147-5975(87)90024-7

Lagrange H, Jay-Allgmand C, Lapeyrie F. Rutin, the phenolglycoside from eucalyptus root exudates, stimulates Pisolithus hyphal growth at picomolar concentrations. New Phytol. 2001;149(2):349–355. https://doi.org/10.1046/j.1469-8137.2001.00027.x

Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, et al. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant–fungus interactions. Molecules. 2007;12(7):1290–1306. https://doi.org/10.3390/12071290

Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 2013;198(1):190–202. https://doi.org/10.1111/nph.12146

Garcia K, Delaux PM, Cope KR, Ané JM. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. New Phytol. 2015;208:79–87. https://doi.org/10.1111/nph.13423

Martinez C, Buée M, Jauneau A, Bécard G, Dargent R, Roux C. Effects of a fraction from maize root exudates on haploid strains of Sporisorium reilianum f. sp. zeae. Plant Soil. 2001;236(2):145–153. https://doi.org/10.1023/A:1012776919384

Sabbagh SK. Effect of GR24, a synthetic analogue of strigolactones, on gene expression of solopathogenic strain of Sporisorium reilianum. Afr J Biotechnol. 2011;10(70):15739–15743. https://doi.org/10.5897/AJB11.393

Sato D, Awad AA, Takeuchi Y, Yoneyama K. Confirmation and quantification of strigolactones, germination stimulants for root parasitic plants Striga and Orobanche, produced by cotton. Biosci Biotechnol Biochem. 2005;69(1):98–102. https://doi.org/10.1271/bbb.69.98