Strigolactones: A New Class of Plant Hormones with Multifaceted Roles

Abstract

Strigolactones (SLs) are terpenoid lactones produced mainly in plant roots and initially identified as seed germination stimulants for parasitic weeds. In 2005, they were described also as boosters of hyphal branching in arbuscular mycorrhizal fungi, and thereby as promoters of arbuscular mycorrhizal symbiosis. In 2008, they emerged as a new class of plant hormones controlling plant architecture through repression of shoot branching. Since then, several new roles were discovered for SLs: in the adaptive responses to a number of environmental stimuli (including light, osmotic stress, interaction with pathogens and nodulating bacteria), and in several aspects of plant development (including seed germination for nonparasitic plants, hypocotyl elongation, reproduction, leaf senescence and nodulation). The biosynthetic and perception/transduction systems of SLs are being elucidated, and the first mechanistic models presented.

Key Concepts:

  • Strigolactones are the key nutrient allocators regulating plant development at the interface between plants, beneficial and detrimental (micro)organisms, and abiotic factors.

  • Strigolactones induce hyphal branching in AM fungi and facilitate the establishment of symbiosis.

  • Strigolactones inhibit shoot branching.

  • Strigolactones affect root architecture and root development depending on nutrients availability.

  • Synthetic SLs (analogues and mimics) are used in pharmacological applications to plants and fungi to decipher the structure–activity relationship.

  • Structure–activity relationship (SAR): Different structures are tested for bioactivity in order to pinpoint which part of the molecule is essential for bioactivity and which can be considered only ‘decoration’.

Keywords: strigolactones; plant hormones; plant development; symbiosis; AM fungi; parasitic plants; shoot branching; hyphal branching; biofertilisers

Figure 1.

Naturally occurring SLs. Natural SLs can be grouped into two families. In one, the absolute configuration of the BCD part (stereochemistry at C3a, C8b and C2′) is the same as parent (+)‐strigol (1); in the other, the stereochemistry is the same as in (−)‐orobanchol (6) (found also in fabyl acetate, ent‐2′‐epi‐orabanchyl acetate and ent‐2′‐epi‐solanacol). In both the families of natural SLs the stereochemistry at C‐2′ remains the same as strigol.

Figure 2.

Some synthetic analogues and mimics of SLs. The difference between analogues and mimics lies on the functional group linked to the D ring. In analogues, as in natural SLs, the D ring is connected to the main core of the molecule through an enol ether bridge (O linked to a double bond). In mimics the D ring is linked to a simpler structure.

Figure 3.

The SL biosynthetic pathway. SLs are derived from carotenoids, and the first steps of their biosynthesis occur in plastids. The main gene products involved in the pathway are indicated; their functions are commented in the text.

Figure 4.

The proposed model of SL perception and signal transduction. D14 binds the SL molecule, hydrolises it and thereby becomes competent to interact with MAX2. MAX2 is an F‐box protein and part of the SCF (Skp, Cullin, F‐box complex) of the proteasome; its interaction with MAX2 in the presence of SLs makes it able to recruit its substrate(s), the repressor proteins of SL responses such as D53 in rice. Once ubiquitinylated, the repressor is committed to be degraded by the proteasome thus initiating signal transduction.

close

References

Agusti J and Greb T (2013) Going with the wind‐adaptive dynamics of plant secondary meristems. Mechanisms of Development 130(1): 34–44.

Akiyama K, Matsuzaki K and Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043): 824–827.

Akiyama K, Ogasawara S, Ito S and Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant and Cell Physiology 51(7): 1104–1117.

Alder A, Jamil M, Marzorati M et al. (2012) The path from beta‐carotene to carlactone, a strigolactone‐like plant hormone. Science 335(6074): 1348–1351.

Bhattacharya C, Bonfante P, Deagostino A et al. (2009) A new class of conjugated strigolactone analogues with fluorescent properties: synthesis and biological activity. Organic and Biomolecular Chemistry 7(17): 3413–3420.

Boyer F‐D, de Saint Germain A, Pillot J-P et al. (2012) Structure–activity relationship studies of strigolactone‐related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiology 159(4): 1524–1544.

Brewer PB, Dun EA, Ferguson BJ, Rameau C and Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiology 150(1): 482–493.

Bu Q, Lv T, Shen H et al. (2014) Regulation of drought tolerance by the F‐box protein MAX2 in Arabidopsis. Plant Physiology 164: 424–439.

Cheng X, Ruyter‐Spira C and Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Frontiers in Plant Science 4: 199–205.

Domagalska MA and Leyser O (2011) Signal integration in the control of shoot branching. Nature Reviews: Molecular Cell Biology 12(4): 211–221.

Dor E, Yoneyama K, Wininger S et al. (2011) Strigolactone deficiency confers resistance in tomato line Sl‐ORT1 to the parasitic weeds Phelipanche and Orobanche spp. Phytopathology 101(2): 213–222.

Foo E, Yoneyama K, Hugill CJ, Quittenden LJ and Reid JB (2012) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Molecular Plant 6(1): 76–87.

Fukui K, Ito S and Asami T (2013) Selective mimics of strigolactone actions and their potential use for controlling damage caused by root parasitic weeds. Molecular Plant 6(1): 88–99.

Gaiji N, Cardinale F, Prandi C, Bonfante P and Ranghino G (2012) The computational‐based structure of Dwarf14 provides evidence for its role as potential strigolactone receptor in plants. BMC Research Notes 5: 307.

Genre A, Chabaud M, Balzergue C et al. (2013) Short‐chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198(1): 190–202.

Guo S, Xu Y, Liu H et al. (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nature Communications 4: 1566.

Ha CV, Leyva-González MA, Osakabe Y et al. (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proceedings of the National Academy of Sciences of the USA 111(2): 851–856.

Janssen BJ and Snowden KC (2012) Strigolactone and karrikin signal perception: receptors, enzymes, or both? Frontiers in Plant Science 3: 296.

Jiang L, Liu X, Xiong G et al. (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504(7480): 401–405.

Johnson X, Brcich T, Dun EA et al. (2006) Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long‐distance signals. Plant Physiology 142(3): 1014–1026.

Kapulnik Y, Resnick N, Mayzlish-Gati E et al. (2011) Strigolactones interact with ethylene and auxin in regulating root‐hair elongation in Arabidopsis. Journal of Experimental Botany 62(8): 2915–2924.

Kelley DR and Estelle M (2012) Ubiquitin‐mediated control of plant hormone signaling. Plant Physiology 160: 147–155.

Kretzschmar T, Kohlen W, Sasse J et al. (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483: 341–346.

Liu J, Lovisolo C, Schubert A and Cardinale F (2013a) Signaling role of strigolactones at the interface between plants, (micro)organisms, and a changing environment. Journal of Plant Interactions 8(1): 17–33.

Liu J, Novero M, Charnikhova T et al. (2013b) CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. Journal of Experimental Botany 64(7): 1967–1981.

Lopez‐Raez JA, Kohlen W, Charnikhova T et al. (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytologist 187(2): 343–354.

Mayzlish‐Gati E, De‐Cuyper C, Goormachtig S et al. (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiology 160(3): 1329–1341.

Nakamura H, Xue YL, Miyakawa T et al. (2013) Molecular mechanism of strigolactone perception by DWARF14. Nature Communications 4: 2613.

Prandi C, Occhiato EG, Tabasso S et al. (2009) New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. European Journal of Organic Chemistry 20–21: 3781–3793.

Rasmussen A, Depuydt S, Goormachtig S and Geelen D (2013) Strigolactones fine‐tune the root system. Planta 238(4): 615–626.

Ruyter‐Spira C, Al‐Babili S, van der Krol S and Bouwmeester H (2013) The biology of strigolactones. Trends in Plant Science 18(2): 72–83.

Ruyter‐Spira C, Kohlen W, Charnikhova T et al. (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiology 155(2): 721–734.

de Saint Germain A, Bonhomme S, Boyer FD and Rameau C (2013) Novel insights into strigolactone distribution and signalling. Current Opinion in Plant Biology 16(5): 583–589.

de Saint Germain A, Ligerot Y, Dun EA et al. (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiology 163(2): 1012–1025.

Torres‐Vera R, García JM, Pozo MJ and López-Ráez JA (2014) Do strigolactones contribute to plant defence? Molecular Plant Pathology 15(2): 211–216.

Tsuchiya Y and McCourt P (2012) Strigolactones as small molecule communicators. Molecular Biosystems 8(2): 464–469.

Ueno K, Nomura S, Muranaka S et al. (2011) Ent‐2 ′‐epi‐orobanchol and its acetate, as germination stimulants for Striga gesnerioides seeds isolated from cowpea and red clover. Journal of Agricultural and Food Chemistry 59(19): 10485–10490.

Umehara M (2011) Strigolactone, a key regulator of nutrient allocation in plants. Plant Biotechnology 28(5): 429–437.

Wang Y, Sun S, Zhu W et al. (2013) Strigolactone/MAX2‐induced degradation of Brassinosteroid transcriptional effector BES1 regulates shoot branching. Developmental Cell 27(6): 681–688.

Xie X, Yoneyama K and Yoneyama K (2010) The strigolactone story. Annual Review of Phytopathology 48: 93–117.

Yoneyama K, Xie X, Kim HI et al. (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235(6): 1197–1207.

Yoshida S, Kameoka H, Tempo M et al. (2012) The D3 F‐box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytologist 196(4): 1208–1216.

Zhou F, Lin Q, Zhu L et al. (2013) D14‐SCFD3‐dependent degradation of D53 regulates strigolactone signalling. Nature 504(7480): 406–410.

Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G and Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Management Science 65(5): 478–491.

Zwanenburg B and Pospisil T (2013) Structure and activity of strigolactones: new plant hormones with a rich future. Molecular Plant 6(1): 38–62.

Further Reading

Bonfante P and Requena N (2013) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 14: 451–457.

Bouwmeester HJ, Roux C, Lopez‐Raez JA and Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends in Plant Science 12: 224–230.

Brewer PB, Koltai H and Beveridge CA (2013) Diverse roles of strigolactones in plant development. Molecular Plant 6: 18–28

Nadal M and Paszkowski U (2013) Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 16: 473–479.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Prandi, Cristina, and Cardinale, Francesca(Apr 2014) Strigolactones: A New Class of Plant Hormones with Multifaceted Roles. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023754]