Structural analysis of HTL and D14 proteins reveals the basis for ligand selectivity in Striga

Xu, Yuqun; Miyakawa, Takuya; Nosaki, Shohei; Nakamura, Akira; Lyu, Y.; Nakamura, Hidemitsu; Ohto, Umeharu; Ishida, Hanako; Shimizu, Toshiyuki; Asami, Tadao; Tanokura, Masaru

doi:10.1038/s41467-018-06452-2

Cited by 78 publications

(119 citation statements)

References 56 publications

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“…Ligand specificity is a key contributor to the functional distinction between karrikin and strigolactone receptors, and elucidating the molecular mechanisms behind ligand specificity is a significant research challenge. In certain root-parasitic weeds in the Orobanchaceae, substitutions of bulky residues found in AtKAI2 with smaller hydrophobic amino acids that increase the ligand-binding pocket size have likely improved the affinity for host-derived strigolactone ligands, as opposed to the smallersized karrikin-type ligands [57][58][59] . Moreover, lid-loop residues that affect the rigidity and size of the ligand entry tunnel determine the ligand selectivity between KAR 1 and ent-5-deoxystrigol (a strigolactone analogue with non-natural stereochemistry) among eleven KAI2 homologues in Physcomitrella patens 60 .…”

Section: Discussionmentioning

confidence: 99%

Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds

et al. 2020

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Wildfires can encourage the establishment of invasive plants by releasing potent germination stimulants, such as karrikins. Seed germination of Brassica tournefortii, a noxious weed of Mediterranean climates, is strongly stimulated by KAR 1 , the archetypal karrikin produced from burning vegetation. In contrast, the closely-related yet non-fire-associated ephemeral Arabidopsis thaliana is unusual because it responds preferentially to KAR 2. The α/β-hydrolase KARRIKIN INSENSITIVE 2 (KAI2) is the putative karrikin receptor identified in Arabidopsis. Here we show that B. tournefortii expresses three KAI2 homologues, and the most highlyexpressed homologue is sufficient to confer enhanced responses to KAR 1 relative to KAR 2 when expressed in Arabidopsis. We identify two amino acid residues near the KAI2 active site that explain the ligand selectivity, and show that this combination has arisen independently multiple times within dicots. Our results suggest that duplication and diversification of KAI2 proteins could confer differential responses to chemical cues produced by environmental disturbance, including fire.

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Section: Discussionmentioning

confidence: 99%

Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds

et al. 2020

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“…In contrast to previous results 37,38 , D-OH induced S. hermonthica germination (EC 50 = 1.2 μM). Moreover, in Arabidopsis lines expressing a GFP fused to ShHTL7, the known S. hermonthica SL receptor 30,39 , was induced by (±)-DOH (EC 50 = 3.1 μM) (Supplementary Figure 14, Supplementary Table 1). In summary, our study validates the perception of D-OH by SL receptors in root-parasitic plants.…”

Section: Resultsmentioning

confidence: 99%

APhelipanche ramosaKAI2 Protein Perceives enzymatically Strigolactones and Isothiocyanates

Germain¹,

Jacobs²,

Brun³

et al. 2020

Preprint

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22Phelipanche ramosa is an obligate root-parasitic weed threatening major crops in central 23Europe. For its germination, it has to perceive various structurally diverging host-exuded 24 signals, including isothiocyanates (ITCs) and strigolactones (SLs). However, the receptors 25 involved are still uncharacterized. Here, we identified five putative SL receptors in P. ramosa, 26 of which PrKAI2d3 is involved in seed germination stimulation. We established the high 27 plasticity of PrKAI2d3, allowing interaction with different chemicals, including ITCs. The SL 28 perception mechanism of PrKAI2d3 is similar to that of endogenous SLs in non-parasitic 29 plants. We provide evidence that the PrKAI2d3 enzymatic activity confers hypersensitivity to 30SLs. Additionally, we demonstrated that methylbutenolide-OH binds PrKAI2d3 and 31 stimulates P. ramosa germination with a bioactivity comparable to that of ITCs. This study 32 highlights that P. ramosa has extended its signal perception system during evolution, a fact to 33 be considered in the development of specific and efficient biocontrol methods. 34Besides their involvement in germination, SLs have a strong stimulating activity on 54 arbuscular mycorrhizal fungi (Glomeromycotina) by promoting mitochondrial metabolism 55 and hyphal branching 7 , thereby mediating the establishment of the oldest mutualistic 56 interaction of land plants 8 . In addition to their role in rhizosphere signaling, SLs act as 57 hormones in planta with pervasive roles throughout the plant development ,9 and, as such, are 58 perceived in vascular plants by the α/β-hydrolase DWARF14 (D14) 10,11 . Biochemical 59 analyses with recombinant D14 proteins by means of the synthetic SL analog GR24 revealed 60 that the SL signal transduction requires GR24 cleavage 11,12 . One of the cleavage products, the 61 D ring, may remain covalently attached to the receptor 13,14 , thereby probably allowing the 62 recruitment of partners for downstream processes 15,16 . The required SL cleavage for signal 63 transduction is still under debate 15,16 . 64 In Arabidopsis thaliana, D14 belongs to a small gene family, including KARRIKIN 65 INSENSITIVE2/HYPOSENSITIVE TO LIGHT (AtKAI2/AtHTL) that shares the α/β-66 hydrolase catalytic triad. However, AtKAI2 regulates AtD14-independent processes, such as 67 seed germination, and preferentially perceives (−)-GR24 that mimics non-natural SLs, 68 karrikins 17 , and supposedly a still unknown endogenous ligand 18 . Interestingly, the KAI2 gene 69 family has expanded during the evolution of obligate parasitic-plant genomes 19 . For example, 70Phelipanche aegyptiaca and Striga hermonthica possess five and eleven KAI2/HTL genes, 71 respectively. Two KAI2 paralogs play a role in SL response in P. aegyptiaca 19 and six S. 72 hermonthica KAI2/HTL proteins are hypersensitive to SLs 19,20 , with ShHTL7 exhibiting the 73 same perception mechanism as D14 21 . The remarkable expansion of the KAI2 gene family in 74Orobanchaceae along with the capacity of P. ramosa to perceive ITCs let us...

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“…There are subtle differences between the unbound forms of D14 and KAI2 that are presumed to determine ligand specificities (Kagiyama et al, 2013;Zhao et al, 2013). In both Arabidopsis and rice, D14 has a larger binding pocket than KAI2 (Kagiyama et al, 2013;Zhao et al, 2013;Xu et al, 2016), which is also seen in Striga D14-like ShHTL proteins that perceive SL, which have consistently larger pockets than KAI2like ShHTL proteins that perceive KAR (Xu et al, 2016(Xu et al, , 2018. These differences are due to the replacement of some of the pocketforming residues with bulkier ones, particularly within the cap, and the closer position of the cap domain relative to the protein core (Kagiyama et al, 2013;Zhao et al, 2013Zhao et al, , 2015Xu et al, 2016Xu et al, , 2018Hameed et al, 2018;Lee et al, 2018;Burger et al, 2019).…”

Section: On the Doorstep: Ligand-receptor Bindingmentioning

confidence: 96%

Fellowship of the rings: a saga of strigolactones and other small signals

2019

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Strigolactones are an important class of plant signalling molecule with both external rhizospheric and internal hormonal functions in flowering plants. The past decade has seen staggering progress in strigolactone biology, permitting highly detailed understanding of their signalling, synthesis and biological rolesor so it seems. However, phylogenetic analyses show that strigolactone signalling mediated by the D14-SCF MAX2-SMXL7 complex is only one of a number of closely related signalling pathways, and is much less ubiquitous in land plants than might be expected. The existence of closely related pathways, such as the KAI2-SMAX1 module, challenges many of our assumptions about strigolactones, and in particular emphasises how little we understand about the specificity of strigolactone signalling with respect to related signalling pathways. In this review, we examine recent advances in strigolactone signalling, taking a holistic evolutionary view to identify the ambiguities and uncertainties in our understanding. We highlight that while we now have highly detailed molecular models for the core mechanism of D14-SMXL7 signalling, we still do not understand the ligand specificity of D14, the specificity of its interaction with SMXL7, nor the specificity of SMXL7 function. Our analysis therefore identifies key areas requiring further study.

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Structural analysis of HTL and D14 proteins reveals the basis for ligand selectivity in Striga

Cited by 78 publications

References 56 publications

Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds

Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds

APhelipanche ramosaKAI2 Protein Perceives enzymatically Strigolactones and Isothiocyanates

Fellowship of the rings: a saga of strigolactones and other small signals

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