Review
Strigolactones in Plant Interactions with Beneficial and Detrimental Organisms: The Yin and Yang

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Central players in regulating plant interactions with beneficial and parasitic organisms are specific compounds exuded by the host plants. SLs are one such group of external signals, with the added intrigue that they also function in planta as phytohormones. Recent advances in our understanding of SL biosynthesis, transport, and perception, as well as of their role in symbiotic and defense pathways may allow the regulation of plant interactions à la carte to encourage beneficial associations, while avoiding harmful ones.

Each plant produces a specific mixture of different SLs. Future research efforts should focus on the action of individual SLs and/or their specific receptors to further explore their targeted uses in agriculture.

Multidisciplinary research on SLs, combining physiological, microbiological, genetic, and molecular approaches, is required to develop new agronomic strategies based on the regulation and/or manipulation of their biosynthesis and/or their signaling pathways.

Strigolactones (SLs) are plant hormones that have important roles as modulators of plant development. They were originally described as ex planta signaling molecules in the rhizosphere that induce the germination of parasitic plants, a role that was later linked to encouraging the beneficial symbiosis with arbuscular mycorrhizal (AM) fungi. Recently, the focus has shifted to examining the role of SLs in plant–microbe interactions, and has revealed roles for SLs in the association of legumes with nitrogen-fixing rhizobacteria and in interactions with disease-causing pathogens. Here, we examine the role of SLs in plant interactions with beneficial and detrimental organisms, and propose possible future biotechnological applications.

Section snippets

The Plant Microbiome

Plants interact with a range of organisms both above- and belowground. Aboveground, plants may interact with microbes, insect herbivores, birds, and other plants that constitute the phyllosphere (see Glossary) and influence plant growth and development 1, 2. Belowground, plant roots grow in a highly dynamic environment containing fungi, bacteria, nematodes, invertebrates, parasitic plants, and the roots of neighboring plants (Figure 1, Key Figure). In particular, the specific rhizosphere

Strigolactones: Multifunctional Molecules in Action

SLs act in planta to regulate shoot branching and root system architecture, adventitious root formation, secondary growth, and leaf senescence (reviewed in [9]). They also contribute to plant responses to nutritional stress, especially phosphorous (P) deprivation 9, 10. More recently, they have also been associated with other abiotic stresses, such as drought and salinity, and even to biotic stress, as we discuss below 11, 12, 13, 14. SLs are apocarotenoids, a class of biologically important

Arbuscular Mycorrhizal Symbiosis

SLs present in root exudates attract AM fungi of the Glomeromycota during the presymbiotic phase (Figure 1 and Table 1), both by enhancing the germination of spores and metabolic activity, and by promoting AM fungal hyphal branching to increase the chance of contact between the hyphae and the host root 32, 33, 34, 35. The development of AM symbiosis dates back more than 450 million years and is considered a crucial step in the evolution of land plants [36]. The symbiosis helps host plants to

Root Parasitic Plants

As mentioned above, SLs were first identified during the 1960s as chemical cues for root parasitic plants of the Orobanchaceae to detect host plants (Figure 1 and Table 1). The SL strigol was identified as a germination stimulant for the parasitic plant Striga spp. [69]. These parasitic weeds, including the genera Striga, Orobanche, and Phelipanche, are obligate parasites that require a host to supply a carbon source within a few days of germination. They are major threats to agriculture,

Strigolactones Interact with Plant Defense Phytohormones

Some of the studies described above suggest that SLs, rather than having a direct effect on the growth or development of pathogenic organisms, interact in planta with other plant defense hormones to influence disease development. Indeed, there are reports of interactions of SL with other plant hormones, although these interactions may vary depending on the developmental process and tissue type [9]. For example, reduced levels of the defense hormones JA, salicylic acid (SA), and ABA were found

Concluding Remarks and Future Perspectives

One of the major challenges for agriculture in the near future is to find more sustainable and environmentally friendly alternatives to reduce the use of chemical fertilizers and pesticides without compromising yield and food quality. One strategy is to harness interactions with beneficial soil microorganisms, including AM fungi and N-fixing rhizobia, that may reduce the need for fertilizers, while increasing crop resilience against diverse stresses under field conditions (see Outstanding

Acknowledgments

The authors thank James B. Reid for critical reading of the manuscript. Research carried out by the authors is supported by the grants AGL2015-64990-C2-1-R from the National R&D Plan of the Ministry of Economy and Competitiveness (MINECO) to J.A.L-R., MEXT KAKENHI grants (No, 24228008 and 15H05959) to K.S., and FF140100770 from the Australian Research Council (ARC) to E.F.

Glossary

Arbuscular mycorrhizal (AM) symbiosis
a mutualistic plant association established between soil fungi of the phylum Glomeromycota and most land plants. This symbiosis facilitates the uptake of water and nutrients by the host plant.
Biofertilizers
microorganisms that, when applied to seeds, plant surfaces, or soil, colonize the rhizosphere or the root system, promoting plant growth by increasing the supply of nutrients to the host plant.
Bioprotection agents
microorganisms that protect plant-based

References (98)

  • J. Sasse

    Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport

    Curr. Biol.

    (2015)
  • N. Mori

    Carlactone-type strigolactones and their synthetic analogues as inducers of hyphal branching in arbuscular mycorrhizal fungi

    Phytochemistry

    (2016)
  • E. Foo

    Auxin influences strigolactones in pea mycorrhizal symbiosis

    J. Plant Physiol.

    (2013)
  • M.J. Soto

    First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa)

    Soil Biol. Biochem.

    (2010)
  • M.A. Peláez-Vico

    Strigolactones in the Rhizobium-legume symbiosis: stimulatory effect on bacterial surface motility and down-regulation of their levels in nodulated plants

    Plant Sci.

    (2016)
  • E. Foo

    Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency

    Mol. Plant

    (2013)
  • J.A. López-Ráez

    Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato

    J. Plant Physiol.

    (2011)
  • A.M. Hooper

    Isoschaftoside, a C-glycosylflavonoid from Desmodium uncinatum root exudate, is an allelochemical against the development of Striga

    Phytochemistry

    (2010)
  • Z.R. Khan

    Combined control of Striga hermonthica and stemborers by maize-Desmodium spp intercrops

    Crop Prot.

    (2006)
  • S. Toh

    Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system

    Chem. Biol.

    (2014)
  • R. Torres-Vera

    Expression of molecular markers associated to defense signaling pathways and strigolactone biosynthesis during the early interaction tomato-Phelipanche ramosa

    Physiol. Mol. Plant Pathol.

    (2016)
  • A. Biere et al.

    Plant-mediated systemic interactions between pathogens, parasitic nematodes, and herbivores above- and belowground

    Annu. Rev. Phytopathol.

    (2015)
  • A. Pineda

    Above–belowground interactions involving plants, microbes and insects

    Front. Plant Sci.

    (2015)
  • J.E. Pérez-Jaramillo

    Impact of plant domestication on rhizosphere microbiome assembly and functions

    Plant Mol. Biol.

    (2016)
  • S. Al-Babili et al.

    Strigolactones, a novel carotenoid-derived plant hormone

    Annu. Rev. Plant Biol.

    (2015)
  • B. Andreo-Jiménez

    Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground

    Plant Soil

    (2015)
  • J.A. López-Ráez

    How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis?

    Planta

    (2016)
  • R. Torres-Vera

    Do strigolactones contribute to plant defence?

    Mol. Plant Pathol.

    (2014)
  • I. Visentin

    Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato

    New Phytol.

    (2016)
  • G.R. Flematti

    Stereospecificity in strigolactone biosynthesis and perception

    Planta

    (2016)
  • M.T. Waters

    Strigolactone signaling and evolution

    Annu. Rev. Plant Biol.

    (2017)
  • L.H. Zhao

    Crystal structures of two phytohormone signal-transducing α/β hydrolases: Karrikin-signaling KAI2 and strigolactone-signaling DWARF14

    Cell Res.

    (2013)
  • H. Nakamura

    Molecular mechanism of strigolactone perception by DWARF14

    Nat. Commun.

    (2013)
  • R. Yao

    DWARF14 is a non-canonical hormone receptor for strigolactone

    Nature

    (2016)
  • L. Jiang

    DWARF 53 acts as a repressor of strigolactone signalling in rice

    Nature

    (2013)
  • F. Zhou

    D14-SCF D3 -dependent degradation of D53 regulates strigolactone signalling

    Nature

    (2013)
  • N. Shabek et al.

    Plant ubiquitin ligases as signaling hubs

    Nat. Struct. Mol. Biol.

    (2014)
  • M.T. Waters

    The karrikin response system of Arabidopsis

    Plant J.

    (2014)
  • X.N. Xie

    The strigolactone story

    Annu. Rev. Phytopathol.

    (2010)
  • X. Xie

    Structural diversity of strigolactones and their distribution in the plant kingdom

    J. Pestic. Sci.

    (2016)
  • H. Proust

    Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens

    Development

    (2011)
  • K. Akiyama

    Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi

    Nature

    (2005)
  • A. Besserer

    Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria

    PLoS Biol.

    (2006)
  • T. Kretzschmar

    A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching

    Nature

    (2012)
  • S.E. Smith et al.

    Mycorrhizal Symbiosis

    (2008)
  • M.J. Pozo

    Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses

    New Phytol.

    (2015)
  • V. Gomez-Roldan

    Strigolactone inhibition of shoot branching

    Nature

    (2008)
  • C. Gutjahr

    The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice

    Plant J.

    (2012)
  • W. Kohlen

    The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis

    New Phytol.

    (2012)
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