2023/08/29 by Shinjiro Yamaguchi, Yoshiya Seto, Junko Kyozuka · 1 voice
Agricultural and Biological Sciences · #Legume Nitrogen Fixing Symbiosis #Plant Parasitism and Resistance #Plant and animal studies
paper · pdf · doi:10.1093/pcp/pcad095
openalex publication_date 2023/08/29 · openalex created_date 2025/10/10 · openalex updated_date 2026/07/30
Strigolactones (SLs) are a group of carotenoid-derived signaling molecules. In 2010, the first special issue on SL was published in Plant & Cell Physiology. Since then, research on various aspects of SLs has progressed remarkably. As is often the case in scientific research, new discoveries in SL research are creating new important questions. In this special issue, four review articles highlight the recent important discoveries and discuss future perspectives in the field. In addition, seven original manuscripts report novel findings related to SLs. SL was first discovered in root exudates of cotton as a germination stimulant of root parasitic plants (Cook et al. 1966). SLs were then identified as hyphal branching inducers of arbuscular mycorrhizal fungi (AMF) (Akiyama et al. 2005). Later, SLs were rediscovered as endogenous plant hormones that inhibit shoot branching (Gomez-Roldan et al. 2008, Umehara et al. 2008). This finding allowed researchers to genetically identify components of the SL biosynthesis and signaling pathways using mutants with increased shoot branching. Biochemical analysis of these genetically identified components confirmed their functions in these SL-related pathways. To date, the outline of SL biosynthesis pathways has been elucidated in several plant species (Mashiguchi et al. 2021). Chemical analyses of SLs mainly in root exudates revealed the diversity of SL chemical structures. In many cases, a single plant species produces multiple SL molecules, and different plant species produce different blends of SLs (Yoneyama et al. 2018). It is also interesting to note that different types/classes of enzyme(s) are occasionally used to synthesize the same SL molecule in different plant species. The biological significance of the vast chemical diversity of SLs is a current important question. SL-insensitive mutants with increased shoot branching have been used to identify major components of the SL signaling pathway. In rice, these include the SL receptor D14 that belongs to the α/β-hydrolase superfamily, the repressor protein D53 and the F-box protein D3. It has been investigated and discussed in detail how these proteins act to transduce the signal upon SL perception (Burger and Chory 2020, Guercio et al. 2023). D14 arose by gene duplication of KAI2, a receptor of an unidentified endogenous molecule called the KAI2 ligand (KL), in the common ancestor of seed plants. Thereafter, repressor proteins for SL signaling occurred in angiosperms. Thus, SL and KL signaling evolved gradually through the step-by-step acquisition of specific signaling components. This special issue covers various topics related to SLs, including their roles as communication signals in the rhizosphere and endogenous hormones. Recently, new roles of SLs in plant communication with other soil-borne organisms have been reported. In this issue, Kee et al. (2023) provide a review article that comprehensively covers the roles of SLs in the rhizosphere, including their role as germination stimulants and chemoattractants of root parasitic plants, activators of AMF, communication chemicals between neighboring plants and influencers of the plant microbiome. In another review article, Huizinga and Bouwmeester (2023) focus on the role of host specificity in root parasitic plants of the Orobanchaceae. They describe in detail the current knowledge of the SL receptors in these root parasitic plant seeds (Huizinga and Bouwmeester 2023). Dun et al. (2023) provide another review article describing the current knowledge of SL biosynthesis and progress in identifying the chemical structure of SL as a plant hormone. In addition, new insight into how SLs coordinately regulate shoot branching is shown (Dun et al. 2023). Also, Varshney and Gutjahr (2023) provide an overview of the recent advances in unveiling the function of KAI2. They also discuss the cross talk between KAI2 signaling and other hormones (Varshney and Gutjahr 2023). Root parasitic plants of the Orobanchaceae germinate in response to host-root-derived SLs. The SL receptor proteins were previously identified in an obligate hemiparasitic plant, Striga hermonthica. However, they remained to be identified in an obligate holoparasitic plant, such as Orobanche minor. In this special issue, Takei et al. (2023) analyzed the function of the homologs of S. hermonthica SL receptors in O. minor. They found that some of them can act as the SL receptor, and notably, one of them was found to have a pico-molar range sensitivity toward SLs when expressed in Arabidopsis. These results pave the way for the development of effective tools to artificially control the germination of root parasitic plants. The Arabidopsis KAI2 pathway is involved in the germination step. Accordingly, its knockout mutant showed a delayed germination phenotype. The KAI2 signaling pathway depends on the function of an F-box protein, MAX2, and MAX2-dependent ubiquitination and proteasomal degradation of SMAX1. The SMAX1 protein contains an ETHYLENE RESPONSE FACTOR Amphiphilic Repression (EAR) motif, which is important for its interaction with the transcriptional corepressor, TOPLESS (TPL). TPL often recruits chromatin remodeling factors such as histone deacetylases (HDACs). In this special issue, Temmerman et al. (2023) discovered that some HDAs are involved in the MAX2-dependent germination of Arabidopsis. Further analyses should elucidate the exact function of these HDACs and the mechanism of how KAI2-MAX2-induced gene expression is regulated. Gibberellins are well-known plant hormones that induce seed germination and promote shoot elongation. However, root parasitic plants of the Orobanchaceae have a unique germination mechanism in which host-derived SLs, but not GA, induce germination. In this special issue, Yap and Tsuchiya (2023) successfully uncovered the involvement of GA in promoting the conditioning process in root parasitic plants, including S. hermonthica and O. minor. More precisely, GA was found to promote the expression of SL receptor genes, ShHTLs, in S. hermonthica. This finding might help provide a new strategy to control Striga seed germination, e.g. by applying GA biosynthetic inhibitors. In the crop plant sorghum, a sulfotransferase known as LOW GERMINATION STIMULANT1 (LGS1) was previously identified as an SL biosynthetic enzyme. LGS1 was found to catalyze the conversion from 18-hydroxy carlactonoic acid (18-OH-CLA) to a mixture of 4-deoxyorobanchol (4DO) and its diastereomer, 5-deoxystrigol (5DS) in vitro; however, only 5DS is endogenously produced in sorghum (Yoda et al. 2021). In this special issue, Yoda et al. (2023) discovered an additional component of SL biosynthesis in sorghum, named Sb3500. They found that when LGS1 was co-expressed with Sb3500, which encodes a 2-oxoglutarate-dependent dioxygenase, only 5DS was produced. The results demonstrate that Sb3500 has an important role in catalyzing a stereo-selective cyclization reaction during SL biosynthesis in sorghum. The SL signaling pathway is mediated by the D14 α/β-hydrolase family receptor in rice. When D14 interacts with SLs, it forms a complex with the D3 F-box protein and the D53 repressor protein. This complex formation leads to the proteasomal degradation of D53 in a D3-dependent manner. Liu et al. (2023) reconstructed this receptor complex (D14–D3–D53) in vitro and analyzed the complex structure using cryo-EM. Although the cryo-EM data did not reveal the location of D53, the D14–D3–ASK1 complex structure in the presence of D53 was nonetheless resolved. The result demonstrates no large conformational change compared with the previously reported AtD14-D3-ASK1 complex crystal structure reported by Yao et al. (2016). They also performed hydrogen–deuterium exchange coupled with mass spectrometry (HDX-MS) and uncovered the dynamic conformational changes in the receptor complex (Liu et al. 2023). The SL receptor, D14, is thought to have arisen through gene duplication of KAI2 in the common ancestor of seed plants. In the D14 and KAI2 signaling pathways, the SMXL family proteins function as repressors, and they have also been duplicated during evolution. In seed plants, the SMXL7/8 subclade functions in the D14 pathway, whereas the SMAX1 subclade is the target of KAI2. Intriguingly, gymnosperms contain both D14 and KAI2, but not SMXL78. In this special issue, Kodama et al. (2023) discovered that D14 and KAI2 in gymnosperms perceive SL analogs and KL mimics, respectively, and it seemed that both signals target SMAX1. These findings strongly suggest that gymnosperms represent an important tool to dissect the evolution of the KAI2 and D14 signaling pathways. The KAI2/D14LIKE (D14L) pathway is involved in the perception of the smoke-derived butenolide germination inducer, karrikin, in Arabidopsis. In rice, this pathway is essential for symbiosis with AMF (Gutjahr et al. 2015). A recent study also implicated the involvement of this pathway in the positive regulation of SL biosynthesis (Choi et al. 2020). In this special issue, Mashiguchi et al. (2023) discovered that the SL analogs with non-natural type stereochemistry, such as (−)-GR5, significantly increase SL biosynthesis in a D14L pathway-dependent manner in rice. Moreover, the increase in SL levels by (−)-GR5 was also observed in other mycorrhizal plant species. By contrast, such a phenomenon has not been observed in non-mycorrhizal plant species, such as Arabidopsis, nor in the mycorrhizal basal plant Marchantia paleacea. These results suggest that SL biosynthesis activation by the D14L pathway has a critical role in regulating AM symbiosis and that this system was acquired after the divergence of bryophytes. SL research has been progressing rapidly, but there is still a lot to learn about the biological roles, biosynthesis, transport, perception, signaling and evolution of SLs. For instance, we still do not know the biologically active form of SL as an endogenous hormone. And further studies are required to understand the exact mechanisms of SL perception and signaling in plants. SL receptors in microorganisms have not been clarified yet, and a KL has yet to be identified to better understand its biological functions and evolution. We hope that this special issue will attract the interest of PCP’s broad readership and encourage more researchers to make new discoveries in this active research field. Japan Society for the Promotion of Science KAKENHI (23H05409 to J.K., S.Y. and Y.S. and 22H02276 to Y.S.); Japan Science and Technology Agency FOREST (JPMJFR211S to Y.S.); the International Collaborative Research Program of Institute for Chemical Research, Kyoto University (2023-132 to Y.S.). We thank Professor Wataru Sakamoto, Editor-in-Chief, of Plant & Cell Physiology, for providing the opportunity for this special issue. We also thank Dr Liliana M. Costa, PCP Managing Editor, for her kind support, and to all the authors and reviewers for their great contributions to this special focus issue. The authors have no conflicts of interest to declare.