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Authors: Shannon A. Stirling, Angelica M. Guercio, Ryan M. Patrick, Xing-Qi Huang, Matthew E. Bergman, Varun Dwivedi, Ruy W. J. Kortbeek, Yi-Kai Liu, Fuai Sun, W. Andy Tao, Ying Li, Benoît Boachon, Nitzan Shabek and Natalia Dudareva.
Science (2024)
One-sentence summary: Informational exchange in plants occurs stereospecifically via volatile terpenoids and the KAI2-like signaling pathway.
Editor’s view: Plant responses to chemical signals carried through the air are critical for development, fitness, and adaptation. Stirling et al. identified a mechanism for the perception of the volatile compound (−)-germacrene D through a homolog of the Karrikin receptor KAI2 in petunia pistils. Genetic and biochemical experiments linked this perception with downstream signaling proteins and transcriptional targets. Perturbing the function of some of these components affected volatile-mediated communication and plant fitness.
Abstract: "Plants are constantly exposed to volatile organic compounds (VOCs) that are released during plant-plant communication, within-plant self-signaling, and plant-microbe interactions. Therefore, understanding VOC perception and downstream signaling is vital for unraveling the mechanisms behind information exchange in plants, which remain largely unexplored. Using the hormone-like function of volatile terpenoids in reproductive organ development as a system with a visual marker for communication, we demonstrate that a petunia karrikin-insensitive receptor, PhKAI2ia, stereospecifically perceives the (−)-germacrene D signal, triggering a KAI2-mediated signaling cascade and affecting plant fitness. This study uncovers the role(s) of the intermediate clade of KAI2 receptors, illuminates the involvement of a KAI2ia-dependent signaling pathway in volatile communication, and provides new insights into plant olfaction and the long-standing question about the nature of potential endogenous KAI2 ligand(s)."
Author: Marco Bürger.
The Plant Cell (2024)
Excerpts: "The KAI2 ligand (KL) is one or several unknown signaling molecule(s) involved in important plant processes, potentially representing an unidentified phytohormone. KL signaling, while interconnected with strigolactone (SL) signaling, distinctly influences plant development and photomorphogenesis....... Intriguingly, in the moss Physcomitrium patens, SL signaling is independent of MAX2 (Lopez-Obando et al., 2018), highlighting a unique aspect of this organism’s biology. Previous research has explored multiple KL and SL receptors in P. patens, assigning them to their signaling pathways (Lopez-Obando et al., 2021). In a new study, Ambre Guillory and colleagues (Guillory et al., 2024) now demonstrate that SMXL proteins act as negative growth regulators in P. patens, functioning downstream of MAX2 in the KL signaling pathway."
"These findings provide a deeper understanding of the molecular mechanisms underpinning moss growth regulation. The results support a model in which PpSMXL proteins are integral to the PpMAX2-dependent KL pathway (see Figure) and provide hints at a possible interplay between SL and KL."
Authors: Lior Tal, Angelica M. Guercio, Kartikye Varshney, Aleczander Young, Caroline Gutjahr and Nitzan Shabek.
New Phytologist (2023)
Excerpts: "Given the dual role of D3/MAX2 in SL and KAR/KL signaling pathways, the function of MAX2 CTH in KAR/KL signaling regulation remains to be addressed. Here, we investigate the effects of the CTH dynamics both in vitro and in Arabidopsis and demonstrate a conserved central role for the CTH dynamics between SL and the KAR/KL signaling pathways."
"Indeed, KAI2 hydrolysis was further inhibited in the presence of both D3 and citrate with no effect in the presence of succinate as control (Fig. S4b). Altogether, these results indicate that the CTH dislodged form of D3 plays a role in the interaction with KAI2 in a similar manner as shown with D14 (Shabek et al., 2018; Tal et al., 2022)."
"Notably, among 200 represented sequences of KAI2 and D14 from different species across the phylogeny from algae to angiosperms (Bythell-Douglas et al., 2017), we found high structural similarities and sequence conservations between KAI2, D14 at the predicted interfaces with D3/MAX2 in both the dislodged (Fig. 2d,e) and the engaged (Fig. 2f,g) conformational states. Altogether, these results further corroborate that the CTH conformational state of D3/MAX2-CTH significantly contributes to KAI2 recruitment and subsequent targeting of SMAX1 in the KAR/KL signaling pathway."
Authors: Kyoichi Kodama, Xiaonan Xie, Junko Kyozuka.
Plant and Cell Physiology (2023)
Abstract: "Strigolactones (SLs), lactone-containing carotenoid derivatives, function as signaling molecules in the rhizosphere, inducing symbiosis with arbuscular mycorrhizal. In addition, as a class of plant hormones, SLs control plant growth and development in flowering plants (angiosperms). Recent studies show that the ancestral function of SLs, which precede terrestrialization of plants, is as rhizosphere signaling molecules. SLs were then recruited as a class of plant hormones through the step-by-step acquisition of signaling components. The D14 gene encoding the SL receptor arose by gene duplication of KARRIKIN INSENSITIVE2 (KAI2), the receptor of karrikins and KAI2 ligand (KL), an unknown ligand, in the common ancestor of seed plants. KL signaling targets SMAX1, a repressor protein. On the other hand, the SL signaling targets SMXL78 subclade repressors, which arose by duplication of SMAX1 in angiosperms. Thus, gymnosperms contain the SL receptor D14 but not SMXL78, the SL signaling–specific repressor proteins. We studied two gymnosperm species, ginkgo (Ginkgo biloba) and Japanese umbrella pine (Sciadopitys verticillata), to clarify whether SLs are perceived and the signals are transduced in gymnosperms. We show that D14 and KAI2 of ginkgo and Japanese umbrella pine specifically perceive an SL analog and KL mimic, respectively. Furthermore, our results suggest that both SL signaling and KL signaling target SMAX1, and the specific localization of the receptor may result in the specificity of the signaling in gymnosperms."
Authors: Pil Joon Seo, Hong Gil Lee, Hye-Young Choi, Sangmin Lee and Chung-Mo Park.
Trends in Plant Science (2023)
Highlights The SMAX1 proteins are gradually destabilized upon exposure to warm temperatures and the thermodynamic control of SMAX1 abundance balances the phyB action, thus thermosensitizing the PIF4-dependent hypocotyl morphogenesis. The photo-induced stabilization of SMAX1 represses the nuclear accumulation of DELLA proteins in hypocotyl cells, in which SMAX1 integrates light and KAR signals into the GA-DELLA signaling pathways. The D14-mediated SL signaling pathway and the KAI2-mediated KAR signaling pathway act together to enhance plant tolerance to environmental constraints. SMAX1 lies at the crosstalks of SL and KAR signals and serves as a molecular hub that links various growth hormone signaling cascades with seedling establishment. The protein structural and functional organization and presence of predicted IDRs in the SMAX1 protein suggest that SMAX1 could incorporate multiple cellular and growth hormone signals into optimizing seedling establishment.
Abstract: "Karrikins (KARs) are small butenolide compounds identified in the smoke of burning vegetation. Along with the stimulating effects on seed germination, KARs also regulate seedling vigor and adaptive behaviors, such as seedling morphogenesis, root hair development, and stress acclimation. The pivotal KAR signaling repressor, SUPPRESSOR OF MAX2 1 (SMAX1), plays central roles in these developmental and morphogenic processes through an extensive signaling network that governs seedling responses to endogenous and environmental cues. Here, we summarize the versatile roles of SMAX1 reported in recent years and discuss how SMAX1 integrates multiple growth hormone signals into optimizing seedling establishment. We also discuss the evolutionary relevance of the SMAX1-mediated signaling pathways during the colonization of aqueous plants to terrestrial environments."
Authors: Lingling Yin, Mark Zander, Shao-shan Carol Huang, Mingtang Xie, Liang Song, J. Paola Saldierna Guzmán, Elizabeth Hann, Bhuvana K. Shanbhag, Sophia Ng, Siddhartha Jain, Bart J. Janssen, Natalie M. Clark, Justin Walley, Travis Beddoe, Ziv Bar-Joseph,Mathew G. Lewsey and Joseph R. Ecker.
bioRxiv (2023)
Abstract: "Cross-regulation between hormone signaling pathways is indispensable for plant growth and development. However, the molecular mechanisms by which multiple hormones interact and co-ordinate activity need to be understood. Here, we generated a cross-regulation network explaining how hormone signals are integrated from multiple pathways in etiolated Arabidopsis (Arabidopsis thaliana) seedlings. To do so we comprehensively characterized transcription factor activity during plant hormone responses and reconstructed dynamic transcriptional regulatory models for six hormones; abscisic acid, brassinosteroid, ethylene, jasmonic acid, salicylic acid and strigolactone/karrikin. These models incorporated target data for hundreds of transcription factors and thousands of protein-protein interactions. Each hormone recruited different combinations of transcription factors, a subset of which were shared between hormones. Hub target genes existed within hormone transcriptional networks, exhibiting transcription factor activity themselves. In addition, a group of MITOGEN-ACTIVATED PROTEIN KINASES (MPKs) were identified as potential key points of cross-regulation between multiple hormones. Accordingly, the loss of function of one of these (MPK6) disrupted the global proteome, phosphoproteome and transcriptome during hormone responses. Lastly, we determined that all hormones drive substantial alternative splicing that has distinct effects on the transcriptome compared with differential gene expression, acting in early hormone responses. These results provide a comprehensive understanding of the common features of plant transcriptional regulatory pathways and how cross-regulation between hormones acts upon gene expression."
Authors: Lior Tal, Angelica Miriam Guercio, Kartikye Varshney, Aleczander Young, Caroline Gutjahr and Nitzan Shabek.
bioRxiv (2023)
Abstract: "Karrikins (KARs) are bioactive molecules derived from burning vegetation. Plants perceive KARs through the alpha/beta hydrolase KARRIKIN INSENSITIVE 2 (KAI2) that interacts with the F-box protein ubiquitin ligase MORE AXILLARY GROWTH 2 (MAX2). MAX2 also plays a role in the perception and signal activation by Strigolactone (SL), a phytohormone controlling various developmental processes in plants. SL also acts as a rhizosphere signal to activate arbuscular mycorrhiza fungi that can be exploited by parasitic plants. kai2 knockouts exhibit distinct developmental defects and therefore KAI2 is hypothesized to perceive an unidentified endogenous ligand provisionally termed KAI2-Ligand (KL). Upon KAR/KL perception, the protein complex of KAI2-MAX2 targets SUPPRESSOR OF MAX2-1/2 (SMAX1)/SMXL2 for proteasomal degradation. Despite the identification of the key components KAI2, MAX2, and SMAX1 in KAR/KL signaling, their mode of interaction and regulation remains elusive. Recently, the regulatory function of the conformational switch of MAX2 C-terminal helix (CTH) in SL signaling has been demonstrated however its role in KAR/KL signaling remained unknown. Here we address the function of MAX2-CTH dynamics both in vitro and in planta and show that the central role of CTH is conserved between SL and KAR/KL signaling pathway."
Authors: Peipei Xu, Hu Jinbo and Weiming Cai.
New Phytologist (2022)
Abstract: "Shade affects all aspects of plant growth and development, including seed germination, hypocotyl elongation, petiole growth, leaf hyponasty, and flowering time. Here, we found that mutations in the key Arabidopsis karrikins signal perception-associated KARRIKIN INSENSITIVE 2 (KAI2) gene, encoding an α/β-fold hydrolase, and the MORE AXILLARY GROWTH 2 (MAX2) gene, encoding an F-box protein, led to greater hypocotyl elongation under shade avoidance conditions. We further verified that these phenotypes were caused by perception of the endogenous KAI2-ligands (KLs), and that this phenotype is independent of strigolactone biosynthetic or signaling pathways. Upon perception of a KL, it is probable that the target protein forms a complex with the KAI2/MAX2 proteins, which are degraded through the action of the 26S proteasome. We demonstrated that SUPPRESSOR OF MAX2-1 (SMAX1) is the degradation target for the KAI2/MAX2 complex in the context of shade avoidance. KAI2 and MAX2 require SMAX1 to limit the hypocotyl growth associated with shade avoidance. Treatment with L-kynurenine (Kyn), an inhibitor of auxin accumulation, partially restored elongation of kai2 mutant hypocotyls under simulated shade. Furthermore, KAI2 is involved in regulating auxin accumulation and polar auxin transport, which may contribute to the hypocotyl shade response. In addition, SMAX1 gene overexpression promoted the hypocotyl shade response. RNA-Seq analysis revealed that SMAX1-overexpression affected the expression of many auxin homeostasis genes, especially under simulated shade. Altogether, our data support the conclusion that KL signaling regulates shade avoidance by modulating auxin homeostasis in the hypocotyl."
Authors: Stephanie E. Martinez, Caitlin E. Conn, Angelica M. Guercio, Claudia Sepulveda, Christopher J. Fiscus, Daniel Koenig, Nitzan Shabek and David C. Nelson.
Plant Physiology (2022)
Abstract: "Karrikins (KARs) are chemicals in smoke that can enhance germination of many plants. Lettuce (Lactuca sativa) cv. Grand Rapids germinates in response to nanomolar karrikinolide (KAR1). Lettuce is much less responsive to KAR2 or a mixture of synthetic strigolactone analogs, rac-GR24. We investigated the molecular basis of selective and sensitive KAR1 perception in lettuce. The lettuce genome contains two copies of KARRIKIN INSENSITIVE2 (KAI2), which in Arabidopsis (Arabidopsis thaliana) encodes a receptor that is required for KAR responses. LsKAI2b is more highly expressed than LsKAI2a in dry achenes and during early stages of imbibition. Through cross-species complementation assays in Arabidopsis, we found that an LsKAI2b transgene confers robust responses to KAR1, but LsKAI2a does not. Therefore, LsKAI2b likely mediates KAR1 responses in lettuce. We compared homology models of KAI2 proteins from lettuce and a fire-follower, whispering bells (Emmenanthe penduliflora). This identified pocket residues 96, 124, 139, and 161 as candidates that influence the ligand specificity of KAI2. Further support for the importance of these residues was found through a broader comparison of pocket residues among 281 KAI2 proteins from 184 asterid species. Almost all KAI2 proteins had either Tyr or Phe identity at position 124. Genes encoding Y124-type KAI2 are more broadly distributed in asterids than F124-type KAI2. Substitutions at residues 96, 124, 139, and 161 in Arabidopsis KAI2 produced a broad array of responses to KAR1, KAR2, and rac-GR24. This suggests that the diverse ligand preferences observed among KAI2 proteins in plants could have evolved through relatively few mutations."
Authors: Angelica M. Guercio, Salar Torabi, David Cornu, Marion Dalmais, Abdelhafid Bendahmane, Christine Le Signor, Jean-Paul Pillot, Philippe Le Bris, François-Didier Boyer, Catherine Rameau, Caroline Gutjahr, Alexandre de Saint Germain and Nitzan Shabek.
Communications Biology (2022)
Editor's view: Guercio et al., combine structural biology, biochemistry, and plant biology to reveal the dual functions of evolutionarily diverged Pisum KAI2A and KAI2B as both receptors and enzymes with distinct ligand selectivity, and propose adaptive sensitivity to strigolactone phytohormones by KAI2B. They reported the structures of KAI2 in apo and ligand intermediate -bound states that further illuminate KAI2s catalysis mechanism.
Abstract: "KAI2 proteins are plant α/β hydrolase receptors which perceive smoke-derived butenolide signals and endogenous, yet unidentified KAI2-ligands (KLs). The number of functional KAI2 receptors varies among species and KAI2 gene duplication and sub-functionalization likely plays an adaptative role by altering specificity towards different KLs. Legumes represent one of the largest families of flowering plants and contain many agronomic crops. Prior to their diversification, KAI2 underwent duplication resulting in KAI2A and KAI2B. Here we demonstrate that Pisum sativum KAI2A and KAI2B are active receptors and enzymes with divergent ligand stereoselectivity. KAI2B has a higher affinity for and hydrolyses a broader range of substrates including strigolactone-like stereoisomers. We determine the crystal structures of PsKAI2B in apo and butenolide-bound states. The biochemical, structural, and mass spectra analyses of KAI2s reveal a transient intermediate on the catalytic serine and a stable adduct on the catalytic histidine, confirming its role as a bona fide enzyme. Our work uncovers the stereoselectivity of ligand perception and catalysis by diverged KAI2 receptors and proposes adaptive sensitivity to KAR/KL and strigolactones by KAI2B."
Authors: Angelica Miriam Guercio, Salar Torabi, David Cornu, Marion Dalmais, Abdelhafid Bendahmane, Christine Le Signor, Jean-Paul Pillot, Philippe Le Bris, Francois-Didier Boyer, Catherine Rameau, Caroline Gutjahr, Alexandre de Saint Germain and Nitzan Shabek.
bioRxiv (2021)
Abstract: "KAI2 are plant α/β hydrolase receptors, which perceive smoke-derived butenolide signals (karrikins) and putative endogenous, yet unidentified phytohormones (KAI2-ligands, KLs). The number of functional KAI2 receptors varies among plant species. It has been suggested that KAI2 gene duplication and sub-functionalization plays an adaptative role for diverse environments or ligand diversification by altering the receptor responsiveness to specific KLs. Legumes represent one of the largest families of flowering plants and contain many essential agronomic crops. Prior to legume diversification, KAI2 underwent duplication, resulting in KAI2A and KAI2B. Integrating plant genetics, ligand perception and enzymatic assays, and protein crystallography, we demonstrate that Pisum sativa KAI2A and KAI2B act as receptors and enzymes with divergent ligand stereoselectivity. KAI2B has a stronger affinity than KAI2A towards the KAI2-ligand (-)-GR24 and remarkably hydrolyses a broader range of substrates including the strigolactone-like isomer (+)-GR24. We determine the crystal structures of PsKAI2B in apo and butenolide-bound states. The biochemical and structural analyses as well as recorded mass spectra of KAI2s reveal a transient intermediate on the catalytic serine and a stable adduct on the catalytic histidine, further illuminating the role of KAI2 not only as receptors but also as bona fide enzymes. Our work uncovers the stereoselectivity of ligand perception and catalysis by evolutionarily diverged KAI2 receptors in KAR/KL signaling pathways and proposes adaptive sensitivity to KAR/KL and strigolactone phytohormones by KAI2B."
Authors: Mauricio Lopez-Obando, Ambre Guillory, François-Didier Boyer, David Cornu, Beate Hoffmann, Philippe Le Bris, Jean-Bernard Pouvreau, Philippe Delavault, Catherine Rameau, Alexandre de Saint Germain and Sandrine Bonhomme.
The Plant Cell (2021)
Abstract: "In angiosperms, the α/β hydrolase DWARF14 (D14), along with the F-box protein MORE AXILLARY GROWTH2 (MAX2), perceives strigolactones (SL) to regulate developmental processes. The key SL biosynthetic enzyme CAROTENOID CLEAVAGE DIOXYGENASE8 (CCD8) is present in the moss Physcomitrium patens, and PpCCD8-derived compounds regulate moss extension. The PpMAX2 homolog is not involved in the SL response, but 13 PpKAI2LIKE (PpKAI2L) genes homologous to the D14 ancestral paralog KARRIKIN INSENSITIVE2 (KAI2) encode candidate SL receptors. In Arabidopsis thaliana, AtKAI2 perceives karrikins and the elusive endogenous KAI2-Ligand (KL). Here, germination assays of the parasitic plant Phelipanche ramosa suggested that PpCCD8-derived compounds are likely non-canonical SLs. (+)-GR24 SL analog is a good mimic for PpCCD8-derived compounds in P. patens, while the effects of its enantiomer (−)-GR24, a KL mimic in angiosperms, are minimal. Interaction and binding assays of seven PpKAI2L proteins pointed to the stereoselectivity towards (−)-GR24 for a single clade of PpKAI2L (eu-KAI2). Enzyme assays highlighted the peculiar behavior of PpKAI2L-H. Phenotypic characterization of Ppkai2l mutants showed that eu-KAI2 genes are not involved in the perception of PpCCD8-derived compounds but act in a PpMAX2-dependent pathway. By contrast, mutations in PpKAI2L-G, and -J genes abolished the response to the (+)-GR24 enantiomer, suggesting that PpKAI2L-G, and -J proteins are receptors for moss SLs."
Authors: Katharina Bursch, Ella T. Niemann, David C. Nelson and Henrik Johansson.
The Plant Journal (2021)
Abstract: "The butenolide molecule, karrikin (KAR), emerging in smoke of burned plant material, enhances light responses like germination, inhibition of hypocotyl elongation, and anthocyanin accumulation in Arabidopsis. The KAR signaling pathway consists of KARRIKIN INSENSITIVE 2 (KAI2) and MORE AXILLARY GROWTH 2 (MAX2), which upon activation act in an SCF E3 ubiquitin ligase complex to target the downstream signaling components SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE 2 (SMXL2) for degradation. How degradation of SMAX1 and SMXL2 is translated into growth responses remains unknown. Although light clearly influences the activity of KAR, the molecular connection between the two pathways is still poorly understood. Here we demonstrate that the KAR signaling pathway promotes the activity of a transcriptional module consisting of ELONGATED HYPOCOTYL 5 (HY5), B-BOX DOMAIN PROTEIN 20 (BBX20), and BBX21. The bbx20 bbx21 mutant is largely insensitive to treatment with KAR2, like a hy5 mutant, with regards to inhibition of hypocotyl elongation and anthocyanin accumulation. Detailed analysis of higher order mutants in combination with RNA-seq analysis revealed that anthocyanin accumulation downstream of SMAX1 and SMXL2 is fully dependent on the HY5-BBX module. However, the promotion of hypocotyl elongation by SMAX1 and SMXL2 is, in contrast to KAR2 treatment, only partially dependent on BBX20, BBX21, and HY5. Taken together, these results suggest that light- and KAR-dependent signaling intersect at the HY5-BBX transcriptional module."
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Author: Tom Bennett.
Current Biology (2024)
Summary: RsbQ from bacteria and KAI2 from plants are highly related α/β-hydrolase proteins with unknown ligands. In a new study, Melville, Kamran et al. attempt to understand the ligand binding of RsbQ using knowledge from studies of KAI2, with surprising results.
Excerpts: "Consistent with its status as a member of a well-defined family of enzymes, the RsbQ protein contains a ligand-binding pocket in which a small molecule can bind — a molecule that almost certainly regulates RsbQ activity6. However, the nature of this molecule has never been clear: what is it that turns RsbQ on or off? This is the question that Melville, Kamran and colleagues attempt to answer in their new study. Their interest in RsbQ is perhaps a good example of ‘horizontal interest transfer’, since it originally arose from the study of an α/β-hydrolase in plants, KARRIKIN INSENSITIVE2 (KAI2)."
"Moreover, KAI2 plays important roles in development that are clearly independent of smoke perception. It is therefore assumed that there is another, endogenous ligand for KAI2 — the imaginatively named ‘KAI2 ligand’ — that activates KAI2 signalling in all land plants, and that seed plants have specifically upcycled their KAI2 proteins to also detect karrikins8. However, the identity of this presumed KAI2 ligand remains a closely guarded secret, currently known only to plants themselves."
"The identity of the RsbQ ligand thus remains a secret as closely guarded as the identity of the KAI2 ligand, but the results of the study nevertheless support the idea that KAI2 and RsbQ share a common ancestry and can behave in a similar way in response to the same ligands.
Authors: Takahito Nomura, Yoshiya Seto and Junko Kyozuka.
Journal of Experimental Botany (2024)
Abstract: "Strigolactone (SL) is the collective name for compounds containing a butenolide as a part of their structure, first discovered as compounds that induce seed germination of root parasitic plants. They were later found to be rhizosphere signaling molecules that induce hyphal branching of arbuscular mycorrhizal (AM) fungi, and finally, they emerged as a class of plant hormones. SLs are found in root exudates, where they display a great variability in their chemical structure. Their structure varies among plant species, and multiple SLs can exist in one species. Over 30 SLs have been identified, yet the chemical structure of the SL that functions as an endogenous hormone and is found in the above-ground parts of plants remains unknown. We discuss our current knowledge of the synthetic pathways of diverse SLs and their regulation as well as recent progresses in identifying SLs as plant hormones. SL is perceived by the D14 receptor, an α/β hydrolase which originated by gene duplication of KARRIKIN INSENSITIVE 2 (KAI2). D14 and KAI2 signaling pathways are partially overlapping paralogous pathways. Progress in understanding the signaling mechanisms mediated by two α/β hydrolase receptors as well as remaining challenges in the field of SL research are reviewed."
Authors: Kartikye Varshney and Caroline Gutjahr.
Plant and Cell Physiology (2023)
Abstract: "The α/β hydrolase KARRIKIN INSENSITIVE 2 (KAI2) functions as a receptor for a yet undiscovered phytohormone, provisionally termed KAI2-ligand (KL). In addition, it perceives karrikin, a butenolide compound found in the smoke of burnt plant material. KAI2-mediated signalling is involved in regulating seed germination and in shaping seedling and adult plant morphology, both above and below ground. It also governs responses to various abiotic stimuli and stresses and shapes biotic interactions. KAI2-signalling is being linked to an elaborate cross-talk with other phytohormone pathways such as auxin, gibberellin, abscisic acid, ethylene, and salicylic acid signalling, in addition to light and nutrient starvation signalling. Further connections will likely be revealed in the future. This article summarizes recent advances in unravelling the function of KAI2-mediated signalling and its interaction with other signalling pathways."
Authors: Hiromu Kameoka, Shota Shimazaki, Kiyoshi Mashiguchi, Bunta Watanabe, Aino Komatsu, Akiyoshi Yoda, Yohei Mizuno, Kyoichi Kodama, Masanori Okamoto, Takahito Nomura, Shinjiro Yamaguchi and Junko Kyozuka.
Current Biology (2023)
Editor's view: Kameoka et al. show that DLP1 is a negative regulator of the KAI2 ligand (KL) pathway in M. polymorpha. DLP1 suppresses the KL signal upstream of the signaling pathway. DLP1 exhibits enzymatic activity toward a potential substrate. These results imply that DLP1 is a KL inactivation enzyme.
Highlights: • DLP1 negatively regulates the KAI2 ligand (KL) signal in M. polymorpha • DLP1 acts upstream of the KL signaling pathway • DLP1 retains enzymatic activities • DLP1 homologs in A. thaliana do not play a major role in the KL pathway
Abstract: "Karrikins are smoke-derived butenolides that induce seed germination and photomorphogenesis in a wide range of plants.1,2,3 KARRIKIN INSENSITIVE2 (KAI2), a paralog of a strigolactone receptor, perceives karrikins or their metabolized products in Arabidopsis thaliana.4,5,6,7 Furthermore, KAI2 is thought to perceive an unidentified plant hormone, called KAI2 ligand (KL).8,9 KL signal is transduced via the interaction between KAI2, MORE AXILLARY GROWTH2 (MAX2), and SUPPRESSOR of MORE AXILLARY GROWTH2 1 LIKE family proteins (SMXLs), followed by the degradation of SMXLs.4,7,10,11,12,13,14 This signaling pathway is conserved both in A. thaliana and the bryophyte Marchantia polymorpha.14 Although the KL signaling pathway is well characterized, the KL metabolism pathways remain poorly understood. Here, we show that DIENELACTONE HYDROLASE LIKE PROTEIN1 (DLP1) is a negative regulator of the KL pathway in M. polymorpha. The KL signal induces DLP1 expression. DLP1 overexpression lines phenocopied the Mpkai2a and Mpmax2 mutants, while dlp1 mutants phenocopied the Mpsmxl mutants. Mutations in the KL signaling genes largely suppressed these phenotypes, indicating that DLP1 acts upstream of the KL signaling pathway, although DLP1 also has KL pathway-independent functions. DLP1 exhibited enzymatic activity toward a potential substrate, suggesting the possibility that DLP1 works through KL inactivation. Investigation of DLP1 homologs in A. thaliana revealed that they do not play a major role in the KL pathway, suggesting different mechanisms for the KL signal regulation. Our findings provide new insights into the regulation of the KL signal in M. polymorpha and the evolution of the KL pathway in land plants."
Authors: Ambre Guillory, Mauricio Lopez-Obando, Khalissa Bouchenine, Philippe Le Bris, Alain Lécureuil, Jean-Paul Pillot, Vincent Steinmetz, François-Didier Boyer, Catherine Rameau, Alexandre de Saint Germain and Sandrine Bonhomme.
bioRxiv (2023)
Abstract: "SMXL proteins are a plant-specific clade of type I HSP100/Clp-ATPases. SMXL genes are found in virtually all land plant genomes. However, they have mainly been studied in angiosperms. In Arabidopsis thaliana, three SMXL functional subclades have been identified: SMAX1/SMXL2, SMXL345 and SMXL678. Out of these, two subclades ensure transduction on endogenous hormone signals: SMAX1/SMXL2 are involved in KAI2-ligand (KL) signaling, while SMXL678 are involved in strigolactones (SLs) signaling. Many questions remain regarding the mode of action of these proteins, as well as their ancestral role. In light of recent discoveries in the liverwort Marchantia polymorpha, we addressed this second question by investigating the function of the four SMXL genes of the moss Physcomitrium patens. We demonstrate that PpSMXL proteins are negative regulators of growth, involved in the likely conserved ancestral MAX2-dependent KL signaling pathway. However, PpSMXL proteins expressed in A. thaliana unexpectedly cannot replace SMAX1/SMXL2 function in KL signaling, whereas they can functionally replace SMXL4/5 and restore root growth. Therefore, the molecular function of SMXL could be conserved, but not their interaction network. Moreover, one PpSMXL clade also positively regulates transduction of the SL signal in P. patens, this function most probably having an independent evolutionary origin to angiosperms SMXL678."
Authors: Aino Komatsu, Kyoichi Kodama, Yohei Mizuno, Mizuki Fujibayashi, Satoshi Naramoto and Junko Kyozuka.
Current Biology (2023)
Editor's view: Plants have a remarkable ability to produce clonal plantlets from vegetative organs. Komatsu et al. show that KAI2- dependent signaling of KL, an as-yet identified plant hormone, promotes clonal plantlet formation in the liverwort Marchantia polymorpha. The number of clonal plantlets is modulated by controlling the ON/OFF timing of the KL signaling.
Highlights: • KAI2-dependent signaling promotes gemma cup formation and gemma initiation • The number of gemmae is controlled by modulating the ON/OFF of the KAI2-signaling • The potassium availability affects gemma cup formation • GCAM1 works downstream of the KAI2-dependent signaling to promote vegetative reproduction
Abstract: "In vegetative reproduction of Marchantia polymorpha (M. polymorpha), propagules, called gemmae, are formed in gemma cups. Despite its significance for survival, control of gemma and gemma cup formation by environmental cues is not well understood. We show here that the number of gemmae formed in a gemma cup is a genetic trait. Gemma formation starts from the central region of the floor of the gemma cup, proceeds to the periphery, and terminates when the appropriate number of gemmae is initiated. The MpKARRIKIN INSENSITIVE2 (MpKAI2)-dependent signaling pathway promotes gemma cup formation and gemma initiation. The number of gemmae in a cup is controlled by modulating the ON/OFF switch of the KAI2-dependent signaling. Termination of the signaling results in the accumulation of MpSMXL, a suppressor protein. In the Mpsmxl mutants, gemma initiation continues, leading to the formation of a highly increased number of gemmae in a cup. Consistent with its function, the MpKAI2-dependent signaling pathway is active in gemma cups where gemmae initiate, as well as in the notch region of the mature gemma and midrib of the ventral side of the thallus. In this work, we also show that GEMMA CUP-ASSOCIATED MYB1 works downstream of this signaling pathway to promote gemma cup formation and gemma initiation. We also found that the availability of potassium affects gemma cup formation independently from the KAI2-dependent signaling pathway in M. polymorpha. We propose that the KAI2-dependent signaling pathway functions to optimize vegetative reproduction by adapting to the environment in M. polymorpha.
Authors: Mark T. Waters and David C. Nelson.
New Phytologist (2023)
Abstract: "Karrikins are a class of butenolide compounds found in smoke that were first identified as seed germination stimulants for fire-following species. Early studies of karrikins classified the germination and post-germination responses of many plant species, and investigated crosstalk with plant hormones that regulate germination. The discovery that Arabidopsis thaliana responds to karrikins laid the foundation for identifying mutants with altered karrikin responses. Genetic analysis of karrikin signalling revealed an unexpected link to strigolactones, a class of carotenoid-derived plant hormones. Substantial progress has since been made toward understanding how karrikins are perceived and regulate plant growth, in no small part due to advances in understanding strigolactone perception. Karrikin and strigolactone signalling systems are evolutionarily related and retain a high degree of similarity. There is strong evidence that karrikins (KARs) are natural analogues of an endogenous signal(s), KAI2 ligand (KL), which remains unknown. KAR/KL signalling regulates many developmental processes in plants including germination, seedling photomorphogenesis, and root and root hair growth. KAR/KL signalling also affects abiotic stress responses and arbuscular mycorrhizal symbiosis. Here we summarise the current knowledge of KAR/KL signalling, and discuss current controversies and unanswered questions in this field."
Authors: Bilal Ahmad, Sami Ullah Qadir, Tariq Ahmad Dar, Pravej Alam, Peerzada Yasir Yousuf and Parvaiz Ahmad.
Journal of Plant Growth Regulation (2023)
Abstract: "Plant-derived smoke is a source of several butenolide compounds collectively termed, karrikins (KARs). These have been recognized as a recent class of plant growth regulators associated with diverse phenomena especially seed germination, seedling vigor and other photo-morphogenetic responses. Role of KARs in improving the performance of plants exposed to different environmental constraints has been recognized recently. KARs mitigate oxidative stress in plants caused by salinity, drought, shade and heavy metals by modulating antioxidative metabolism (SOD, POX, GR, APX) and up-regulating the expression of various stress related genes in plants. Such a modulation involves an interplay with different transcription factors and endogenous plant growth regulators predominantly auxins, gibberellins, ethylene and abscisic acid. The present article is an attempt to gain a comprehensive understanding regarding the KARs-induced plant responses. Moreover, role of KARs in plant abiotic stress tolerance, perception of KARs in plants, expression of different enzymes and genes involved in abiotic stress mitigation, their cross-talk with other endogenous hormones under normal and challenging environmental circumstances.
Authors: Claudia Sepulveda, Michael A. Guzmán, Qingtian Li, José Antonio Villaécija-Aguilar, Stephanie E. Martinez, Muhammad Kamran, Aashima Khosla, Wei Liu, Joshua M. Gendron, Caroline Gutjahr, Mark T. Waters and David C. Nelson.
PNAS (2022)
Significance: Karrikins are chemicals in smoke that stimulate regrowth of many plants after fire. However, karrikin responses are not limited to species from fire-prone environments and can affect growth after germination. Putatively, this is because karrikins mimic an unknown signal in plants, KAI2 ligand (KL). Karrikins likely require modification in plants to become bioactive. We identify a gene, KUF1, that appears to negatively regulate biosynthesis of KL and metabolism of a specific karrikin. KUF1 expression increases in response to karrikin or KL signaling, thus forming a negative feedback loop that limits further activation of the signaling pathway. This discovery will advance understanding of how karrikins are perceived and how smoke-activated germination evolved. It will also aid identification of the elusive KL.
Abstract: "Karrikin (KAR) molecules found in smoke stimulate seed germination of many plant species that emerge after fire. Genetic studies in Arabidopsis thaliana have identified core components of the KAR signaling pathway, including an α/β-hydrolase, KARRIKIN INSENSITIVE2 (KAI2), that is required for KAR responses. Although KAI2 is often considered a KAR receptor, recent evidence suggests that KARs may require metabolism to become bioactive signals. In addition to sensing KARs or a KAR-derived signal, KAI2 is thought to recognize an unknown endogenous signal, KAI2 ligand (KL). We generated loss-of-function mutations in KARRIKIN-UP-REGULATED F-BOX1 (KUF1), which is a transcriptional marker of KAR/KL signaling in A. thaliana and other plants. The kuf1 mutant in Arabidopsis shows several phenotypes that are consistent with enhanced activity of the KAI2 pathway, including reduced hypocotyl elongation, enhanced cotyledon expansion in light-grown seedlings, increased root hair density and elongation, and differential expression of KAR/KL-responsive transcriptional markers. Seedling phenotypes of kuf1 are dependent on KAI2 and its signaling partner MORE AXILLARY GROWTH2 (MAX2). Furthermore, kuf1 mutants are hypersensitive to KAR1, but not to other molecules that can signal through KAI2 such as GR24. This implies that kuf1 does not increase the overall responsiveness of the KAI2-dependent signaling pathway, but specifically affects the ability of KAI2 to detect certain signals. We hypothesize that KUF1 imposes feedback inhibition of KL biosynthesis and KAR1 metabolism. As an F-box protein, KUF1 likely participates in an E3 ubiquitin ligase complex that imposes this regulation through polyubiquitylation of a protein target(s)."
Authors: Qingtian Li, Elena Sánchez Martín-Fontecha, Aashima Khosla, Alexandra R. F. White, Sunhyun Chang, Pilar Cubas and David C. Nelson.
Plant Communications (2022)
Abstract: "The phytohormone strigolactone (SL) and smoke-derived karrikins (KARs) have mostly distinct effects on plants despite being perceived through very similar mechanisms. The homologous receptors DWARF14 (D14) and KARRIKIN INSENSITIVE2 (KAI2) mediate SL and KAR responses, respectively, with the F-box protein MORE AXILLARY GROWTH2 (MAX2) by targeting different SMAX1-LIKE (SMXL) family proteins for degradation. These mechanisms are putatively well-insulated, with D14-MAX2 targeting SMXL6, SMXL7, and SMXL8, and KAI2-MAX2 targeting SMAX1 and SMXL2 in Arabidopsis thaliana. Recent evidence challenges this model. We investigated whether D14 can target SMAX1 and whether this occurs naturally. Genetic analysis indicates the SL analog GR24 promotes D14-SMAX1 crosstalk. Although D14 shows weaker interactions with SMAX1 than SMXL2 or SMXL7, D14 mediates GR24-induced degradation of SMAX1 in plants. Osmotic stress triggers SMAX1 degradation, which is protective, through SL biosynthesis and signaling genes. Thus, D14-SMAX1 crosstalk may be beneficial and not simply a vestige of the SL pathway’s evolution."
Author: Marco Bürger
The Plant Cell (2021)
Excerpts: "Bryophytes such as the moss Physcomitrium patens were among the first plants to appear on land and are excellent model systems to study the evolution of SL signaling. In angiosperms, SLs are perceived by the α/β hydrolase DWARF14 (D14). D14 is structurally similar to KARRIKIN INSENSITIVE2 (KAI2), which is mostly involved in seed germination and seedling development. KAI2’s endogenous signal is still unknown and is commonly referred to as KAI2 ligand (KL). In a new study, Mauricio Lopez-Obando, Ambre Guillory, and colleagues (Lopez- Obando et al., 2021) used a combination of P. patens mutants, pharmacological treatments, in-vitro binding assays, and cross-species complementation to dissect the proteins involved in SL versus KL signaling and perception in this moss (see Figure)."
"The work by Lopez-Obando et al. is an important expansion of a previous study describing the structural mechanism for binding of non-natural SLs by members of the P. patens eu-KAI2 clade (Bürger et al., 2019). The identification of protein clades specific for SLs or KL(s) constitutes a significant advancement in our understanding of SL signaling evolution and the developmental biology of P. patens."
Authors: Amir Arellano-Saab, Michael Bunsick, Hasan Al Galib, Wenda Zhao, Stefan Schuetz, James Michael Bradley, Zhenhua Xu, Claresta Adityani, Asrinus Subha, Hayley McKay, Alexandre de Saint Germain, François-Didier Boyer, Christopher S. P. McErlean, Shigeo Toh, Peter McCourt, Peter J. Stogios, and Shelley Lumba.
PNAS (2021)
Significance: Parasitic plants like witchweed cause huge losses in crop yield in Africa. A key part to the success of witchweed is to start its life cycle upon sensing small molecules called strigolactones, which are exuded from roots of host plants into the soil. Witchweed sense host-derived strigolactones through receptors called HTLs. It is thought that the evolutionary origin of HTLs is a receptor called KAI2 in nonparasitic plants, which can respond to different small molecules such as karrikins. By making three changes in the protein sequence of KAI2, this hybrid receptor can now sense both strigolactones and karrikins. These results help in understanding how receptors can evolve to sense different signals and can lead to solutions for combating pesky witchweed.
Abstract: "Uncovering the basis of small-molecule hormone receptors’ evolution is paramount to a complete understanding of how protein structure drives function. In plants, hormone receptors for strigolactones are well suited to evolutionary inquiries because closely related homologs have different ligand preferences. More importantly, because of facile plant transgenic systems, receptors can be swapped and quickly assessed functionally in vivo. Here, we show that only three mutations are required to turn the nonstrigolactone receptor, KAI2, into a receptor that recognizes the plant hormone strigolactone. This modified receptor still retains its native function to perceive KAI2 ligands. Our directed evolution studies indicate that only a few keystone mutations are required to increase receptor promiscuity of KAI2, which may have implications for strigolactone receptor evolution in parasitic plants."
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