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How Do Strigolactones Ameliorate Nutrient Deficiencies in Plants?

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How Do Strigolactones Ameliorate Nutrient Deficiencies in Plants? Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press How Do Strigolactones Ameliorate Nutrient Deficiencies in Plants? Kaori Yoneyama Graduate School of Agriculture, Ehime University, Matsuyama 790-8566, Japan Correspondence: [email protected] Strigolactones (SLs), a group of plant secondary metabolites, play an important role as a host recognition signal for symbiotic arbuscular mycorrhizal (AM) fungi in the rhizosphere. SLs promote symbioses with other beneficial microbes, including root nodule bacteria. Root parasitic weeds also take advantage of SLs as a clue to locate living host roots. In plants, SLs function as plant hormones regulating various growth and developmental processes includ- ing shoot and root architectures. Plants under nutrient deficiencies, especially that of phos- phate, promote SL production and exudation to attract symbionts and to optimize shoot and root architecture. lants produce various organic chemicals. turn, supply carbohydrates to them. Plants do PPrimary metabolites including nucleic acids, not need symbiotic microbes when satisfactory amino acids, sterols, etc., are present in all plant nutrient-rich conditions exist. Therefore, to reg- species and functioning in basic metabolisms. In ulate symbiotic relationships, plants produce contrast, some of secondary metabolites—often and release chemical signals. produced only in very small quantities and rap- The intimate relationship of leguminous idly disappear—had been hypothesized to be plants and nitrogen (N)-fixing rhizobacteria is inessential for plant growth and development. a well-known symbiosis for legumes to obtain N, However, highly sensitive analytical methods one of essential macronutrients. As shown in enabled us to realize the importance of such Figure 1, this symbiosis is initiated by the spe- secondary metabolites as chemical signals with cific chemical signals, flavonoids exuded from which plants, sessile organisms, can adapt their roots of N-limited legume plants. Only the com- sensitivity to everchanging and stressful envi- patible rhizobia partners sense the specific fla- ronments. vonoid molecules and induce the expression of Plants need inorganic nutrients for their nod genes, which stimulate production and survival but they are very often subjected to nu- exudation of the signals, specific lipochito-oli- trient-limited conditions. One of the strategies gosaccharides named nodulation (Nod) factors. for overcoming such a difficulty, plants have de- Then, Nod factors released from the rhizobia veloped several types of symbiotic relationships induce molecular and physiological changes in with microbes to acquire nutrients. Plants ob- the plants (Kouchi et al. 2010; Venkateshwaran tain nutrients from microorganisms and, in et al. 2013), which will be explained later in de- Editor: Pamela C. Ronald Additional Perspectives on Engineering Plants for Agriculture available at www.cshperspectives.org Copyright © 2019 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a034686 1 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press K. Yoneyama N limited Promote Rhizobia Flavonoids Nod gene Molecular change NF receptors Common symbiotic signaling pathway Nod factor (lipochito-oligosaccharides) Physiological change NSP1 NSP2 Root hair curling Ethylene Infection thread formation SLABA Cortical cell division JA N-fixation Figure 1. Nodule development in leguminous plants. The nodule development in leguminous plants commences by organic chemical signal flavonoids exuded from roots of plants subjected to nitrogen (N) deficiency. Then, nodulation (Nod) factor signals, lipochitooligosaccharides released from Rhizobia induce molecular and phys- iological changes of plants to form nodules. Strigolactones (SLs) seem to be related to nodule formation and transcription factors for nodule formation influence SL biosynthesis (see other beneficial functions of SLs in the rhizosphere). fi tail. Root nodules x atmospheric N2 into am- ability, and possible application of SLs for agri- monia, readily available form of N to plants. cultural production is explained. Arbuscular mycorrhizal (AM) fungus is an- other important symbiotic partner for plants. THE DAWN OF THE STRIGOLACTONE AM fungi form symbiotic relationships with STORY >80% of land plants and they supply nutrients especially phosphate to host plants. Strigolac- The history of SLs began with the isolation of tones (SLs) are key chemical signals for the strigol (Fig. 2), the first natural SL, as a germina- plant–AM fungi symbiotic relationship, and tion stimulant of witchweed (Striga lutea), a dev- the objective of this article is to understand astating root parasitic weed (Cook et al. 1966). how plants use SLs to ameliorate nutrient defi- Approximately 1% of angiosperms (3500 to ciencies. 4000 species) are parasitic plants that depend on The discovery of biological functions of SLs their host plants for the supply of part or all of is quite dramatic and SLs are now widely accept- their needs of water, minerals, and photosyn- ed as multifunctional molecules. In this review, a thates (Nickrent et al. 1998). Depending on brief history of SL research is introduced to un- the site of attachment, parasitic plants are divid- derstand various biological functions of SLs. ed into two groups: stem and root parasites. The Then, structural diversity, biosynthetic pathway, root parasites attach to the roots of host plants perception, and signal transduction, regulation and spend most of their lifecycle underground. of SL production/exudation by nutrient avail- There are two important root parasitic weeds, 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a034686 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Strigolactone Nutrient Acquisition Strategy O O O OH O O O O Orobanchol O O O C O O A B O O O O O O O OH D O O O O Strigol O O Fabacyl acetate O O Orobanchyl acetate HO O O O O O O O O O O OH O O O Sorgomol 5-deoxystrigol Solanacol (5DS) Strigol-type Canonical SL Orobanchol-type O O Noncanonical SL O O H O O O O O O O O O O HO O O Heliolactone O Zealactone O O O O Avenaol O O GR24 O Figure 2. The structures of natural strigolactones (SLs) and synthetic analog GR24. witchweeds (Striga spp.) and broomrapes (Oro- Orobanche and Phelipanche spp. are holo- banche and Phelipanche spp.) of Orobancha- parasites, lacking chlorophylls and completely ceae, causing significant damages to agricultural depend on host plants. Their host and habitat production all over the world. ranges are quite wide and they parasitize dicot- Striga spp. are hemiparasites, having func- yledonous crops, including legumes, tomato, tional chloroplasts but obligate parasites, which sunflower, oilseed rape, etc. in temperate areas. cannot complete their lifecycle without parasit- The areas threatened by Orobanche and Pheli- izing their hosts. They parasitize mainly mo- panche, as estimated in 1991, are 16 million nocotyledonous crops, for example, maize, hectares in the Mediterranean and west Asia sorghum, millet, sugarcane, and upland rice in (Parker 2009). tropical areas. The United Nations estimates The problems caused by these root parasitic that Striga is the major constraint to crop pro- weeds are not only a significant reduction of duction in sub-Saharan Africa causing average crop production but also the limitation of crop yield losses of 40%, but total crop failure is com- transportation. Serious root parasites are classi- mon (Ejeta and Gressel 2007). fied as quarantine weeds in most countries, and Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a034686 3 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press K. Yoneyama thus infested lands must be strictly isolated and which induces extensive hyphal branching, a the crops harvested there cannot be exported critical morphogenetical change in host recog- when even a single root parasite is found in nition by AM fungi (Akiyama et al. 2005). These the area. investigators also showed that other natural SLs, A single root parasite can produce up to half sorgolactone and strigol, and the synthetic SL a million tiny seeds that are half the size of Ara- analog GR24 (Fig. 2) induce extensive hyphal bidopsis (approximately 0.3 mm to 0.5 mm). branching in germinating spores of the AM fun- They can survive decades in soils, waiting for gus Gigaspora margarita at very low concentra- their preferable crop hosts. The tiny seeds of tions. Besserer et al. (2006) showed that GR24 root parasites with limited food stock will die also stimulates spore germination and hyphal unless they can parasitize suitable host roots branching of Glomus intraradices and Glomus within a few days after germination. An inge- claroideum through rapid increase of mitochon- nious survival strategy of the root parasites is drial density and respiration. that the seeds can germinate only when they Experiments with SL-deficient mutants perceive germination stimulants released from showed that SLs are essential signaling factors host roots. for plants to form symbiotic relationships with Strigol was isolated as a germination stimu- AM fungi.
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