 Your new post is loading...
Your new post is loading...
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: Kim T. Melville, Muhammad Kamran, Jiaren Yao, Marianne Costa, Madeleine Holland, Nicolas L. Taylor, Georg Fritz, Gavin R. Flematti and Mark T. Waters.
Current Biology (2024)
Editor's view: RsbQ is a bacterial protein homologous to hormone receptors in plants. Melville et al. show that RsbQ from Bacillus subtilis is sensitive to butenolide compounds that serve as plant hormone analogs, and that these compounds promote biofilm formation. Their findings implicate butenolides as potential interkingdom chemical signals.
Highlights • RsbQ perceives butenolide compounds via a conserved catalytic mechanism • Application of exogenous butenolides phenocopy loss of RsbQ function • Butenolides promote biofilm formation in non-domesticated B. subtilis
Abstract: "The regulation of behavioral and developmental decisions by small molecules is common to all domains of life. In plants, strigolactones and karrikins are butenolide growth regulators that influence several aspects of plant growth and development, as well as interactions with symbiotic fungi.1,2,3 DWARF14 (D14) and KARRIKIN INSENSITIVE2 (KAI2) are homologous enzyme-receptors that perceive strigolactones and karrikins, respectively, and that require hydrolase activity to effect signal transduction.4,5,6,7 RsbQ, a homolog of D14 and KAI2 from the gram-positive bacterium Bacillus subtilis, regulates growth responses to nutritional stress via the alternative transcription factor SigmaB (σB).8,9 However, the molecular function of RsbQ is unknown. Here, we show that RsbQ perceives butenolide compounds that are bioactive in plants. RsbQ is thermally destabilized by the synthetic strigolactone GR24 and its desmethyl butenolide equivalent dGR24. We show that, like D14 and KAI2, RsbQ is a functional butenolide hydrolase that undergoes covalent modification of the catalytic histidine residue. Exogenous application of both GR24 and dGR24 inhibited the endogenous signaling function of RsbQ in vivo, with dGR24 being 10-fold more potent. Application of dGR24 to B. subtilis phenocopied loss-of-function rsbQ mutations and led to a significant downregulation of σB-regulated transcripts. We also discovered that exogenous butenolides promoted the transition from planktonic to biofilm growth. Our results suggest that butenolides may serve as inter-kingdom signaling compounds between plants and bacteria to help shape rhizosphere communities."
Authors: Muhammad Kamran, Kim T. Melville, Mark T. Waters.
Journal of Experimental Botany (2024)
Abstract: "Plants rely upon a diverse range of metabolites to control growth and development, and to overcome stress that results from suboptimal conditions. Karrikins (KARs) are a class of butenolide compounds found in smoke that stimulate seed germination and regulate various developmental processes in plants. KARs are perceived via a plant α/β-hydrolase called KARRIKIN INSENSITIVE2 (KAI2), which also functions as a receptor for a postulated phytohormone, provisionally termed KAI2-ligand (KL). Considered natural analogues of KL, KARs have been extensively studied for their effects on plant growth and their crosstalk with plant hormones. The perception and response pathway for KAR-KL signalling is closely related to that of strigolactones, another class of butenolides with numerous functions in regulating plant growth. KAR-KL signalling influences seed germination, seedling photomorphogenesis, root system architecture, abiotic stress responses, and arbuscular mycorrhizal symbiosis. Here, we summarise the current knowledge of KAR-KL signalling, focussing on its role in plant development, its effects on stress tolerance, and its interaction with other signalling mechanisms."
Authors: Suhua Li, Gundega Baldwin, Caiqiong Yang, Ruirui Lu, Shuaishuai Meng, Jianbei Huang, Ming Wang and Ian T. Baldwin.
Plant, Cell & Environment (2024)
Abstract: "Laboratory studies have revealed that strigolactone (SL) and karrikin (KAR) signalling mediate responses to abiotic and biotic stresses, and reshape branching architecture that could increase reproductive performance and crop yields. To understand the ecological function of SL and KAR signalling, transgenic lines of wild tobacco Nicotiana attenuata, silenced in SL/KAR biosynthesis/signalling were grown in the glasshouse and in two field plots in the Great Basin Desert in Utah over four field seasons. Of the lines silenced in SL and KAR signalling components (irMAX2, irD14, irKAI2 and irD14 × irKAI2 plants), which exhibited the expected increases in shoot branching, only irMAX2 plants showed a strong leaf-bleaching phenotype when grown in the field. In the field, irMAX2 plants had lower sugar and higher leaf amino acid contents, lower lifetime fitness and were more susceptible to herbivore attack compared to wild-type plants. These irMAX2 phenotypes were not observed in glasshouse-grown plants. Transcriptomic analysis revealed dramatic responses to high-light intensity in irMAX2 leaves in the field: lutein contents decreased, and transcriptional responses to high-intensity light, singlet oxygen and hydrogen peroxide increased. PAR and UV-B manipulations in the field revealed that the irMAX2 bleaching phenotype is reversed by decreasing PAR, but not UV-B fluence. We propose that NaMAX2 functions in high-light adaptation and fitness optimisation by regulating high-light responses independently of its roles in the SL and KAR signalling pathways. The work provides another example of the value of studying the function of genes in the complex environments in which plants evolved, namely nature."
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: Pinging Fang, Yannan Hu, Qinwei Guo, Lan Li and Pei Xu.
Plant Stress (2023)
Highlights: • The discovery and signaling transduction of KAR is summarized. • An overview of the recent advances in KAR actions under abiotic stress is provided. • The involvement of redox signals in KAR-regulated stress responses is highlighted.
Abstract: Karrikins (KARs) are bioactive butenolide molecules that were initially discovered as germination stimulants in the smoke generated from burned plant materials. The past decades have witnessed the unraveling of KARs as a group of potential plant hormones that impact various aspects of plant physiology, from regulation of light responses and controlling root morphology, to modulation of secondary metabolism. KARs share a similar structure with strigolactones (SLs), and they activate similar signaling pathways where the interaction of α/β hydrolases with the F-box protein MORE AXILLARY GROWTH 2 (MAX2) is involved. Upon binding with KARs, the α/β hydrolase KAI2 (KARRIKIN INSENSITIVE 2) interacts with MAX2, which in turn activates the downstream signals by promoting the degradation of SMAX1/SMXL2 (SUPPRESSOR OF MAX2 1/SMX1-LIKE). Recent accumulating evidence has proved that KARs act as a protective agent regulating plant adaptation to abiotic stresses, particularly drought, salinity, and extreme temperature; however, these functions have not been widely perceived. This review revisits the knowledge of the characteristics and signals transduction of KARs in plants, with a focus on the interplay of KARs and redox signals in modulating plant tolerance to abiotic stresses. This collection of information is valuable for better understanding plant-environment interactions and will help create stress-tolerant crops and achieve the goal of agricultural and ecological sustainability."
Authors: Minghui Liu, Qing Shan, Erqiao Ding, Tingting Gu and Biao Gong.
Plant Science (2023)
Highlights: • Exogenous smoking water and KAR can improve low temperature resistance of tomato plants. • KAR improves cold tolerance of tomato by affecting SLs and ABA signals. • Smoking water and KAR can promote tomato growth, yield and production capacity under long-term sub-low temperature environment
Abstract: "As a class of biostimulants, karrikins (KARs) were first identified from plant-derived smoke to regulate plant growth, development, and stress tolerance. However, the roles of KARs in plant cold tolerance and their crosstalk with strigolactones (SLs) and abscisic acid (ABA) remain elusive. We studied the interaction among KAR, SLs, and ABA in cold acclimatization with KAI2-, MAX1-, SnRK2.5-silenced, or cosilenced plant materials. KAI2 is involved in smoke-water- (SW-) and KAR-mediated cold tolerance. MAX1 acts downstream of KAR in cold acclimation. ABA biosynthesis and sensitivity are regulated by KAR and SLs, which improve cold acclimation through the SnRK2.5 component. The physiological mechanisms of SW and KAR in improving growth, yield, and tolerance under a long-term sublow temperature environment were also studied. SW and KAR were shown to improve tomato growth and yield under sublow temperature conditions by regulating nutritional uptake, leaf temperature control, photosynthetic defense, ROS scavenging, and CBF transcriptional activation. Together, SW, which functions via the KAR-mediated SL and ABA signaling network, has potential application value for increasing cold tolerance in tomato production."
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: Xiujuan Zheng, Fangqian Liu, Xianfeng Yang, Weiqiang Li, Sique Chen, Xinwu Yue, Qi Jia and Xinli Sun.
Journal of Integrative Plant Biology (2023)
Abstract: "Arabidopsis MORE AXILLARY GROWTH2 (MAX2) is a key component in the strigolactone (SL) and karrikin (KAR) signaling pathways and regulates the degradation of SUPPRESSOR OF MAX2 1/SMAX1-like (SMAX1/SMXL) proteins, which are transcriptional co-repressors that regulate plant architecture, as well as abiotic and biotic stress responses. The max2 mutation reduces resistance against Pseudomonas syringae pv. tomato (Pst). To uncover the mechanism of MAX2-mediated resistance, we evaluated the resistance of various SL and KAR signaling pathway mutants. The resistance of SL-deficient mutants and of dwarf 14 (d14) was similar to that of the wild type, whereas the resistance of the karrikin insensitive 2 (kai2) mutant was compromised, demonstrating that the KAR signaling pathway, not the SL signaling pathway, positively regulates the immune response. We measured the resistance of smax1 and smxl mutants, as well as the double, triple, and quadruple mutants with max2, which revealed that both the smax1 mutant and smxl6/7/8 triple mutant rescue the low resistance phenotype of max2 and that SMAX1 accumulation diminishes resistance. The susceptibility of smax1D, containing a degradation-insensitive form of SMAX1, further confirmed the SMAX1 function in the resistance. The relationship between the accumulation of SMAX1/SMXLs and disease resistance suggested that the inhibitory activity of SMAX1 to resistance requires SMXL6/7/8. Moreover, exogenous application of KAR2 enhanced resistance against Pst, but KAR-induced resistance depended on salicylic acid (SA) signaling. Inhibition of karrikin signaling delayed SA-mediated defense responses and inhibited pathogen-induced protein biosynthesis. Together, we propose that the MAX2-KAI2-SMAX1 complex regulates resistance with the assistance of SMXL6/7/8 and SA signaling and that SMAX1/SMXLs possibly form a multimeric complex with their target transcription factors to fine-tune immune responses."
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."
|
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: 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.
The Plant Cell (2024)
Abstract: "SUPPRESSOR OF MAX2 (SMAX)1-LIKE (SMXL) proteins are a plant-specific clade of type I HSP100/Clp-ATPases. SMXL genes are present in virtually all land plant genomes. However, they have mainly been studied in angiosperms. In Arabidopsis (Arabidopsis thaliana), three functional SMXL subclades have been identified: SMAX1/SMXL2, SMXL345 and SMXL678. Of these, two subclades ensure endogenous phytohormone signal transduction. SMAX1/SMXL2 proteins are involved in KAI2 ligand (KL) signaling, while SMXL678 proteins are involved in strigolactone (SL) signaling. Many questions remain regarding the mode of action of these proteins, as well as their ancestral roles. We addressed these questions by investigating the functions of the four SMXL genes in the moss Physcomitrium patens. We demonstrate that PpSMXL proteins are involved in the conserved ancestral MAX2-dependent KL signaling pathway and negatively regulate growth. However, PpSMXL proteins expressed in Arabidopsis cannot replace SMAX1 or SMXL2 function in KL signaling, whereas they can functionally replace SMXL4 and SMXL5 and restore root growth. Therefore, the molecular functions of SMXL proteins are conserved, but their interaction networks are not. Moreover, the PpSMXLC/D clade positively regulates SL signal transduction in P. patens. Overall, our data reveal that SMXL proteins in moss mediate crosstalk between the SL and KL signaling pathways."
Authors: Young-Joon Park, Bo Eun Nam and Chung-Mo Park.
Journal of Integrative Plant Biology (2024)
Abstract: "Coordinated morphogenic adaptation of growing plants is critical for their survival and propagation under fluctuating environments. Plant morphogenic responses to light and warm temperatures, termed photomorphogenesis and thermomorphogenesis, respectively, have been extensively studied in recent decades. During photomorphogenesis, plants actively reshape their growth and developmental patterns to cope with changes in light regimes. Accordingly, photomorphogenesis is closely associated with diverse growth hormonal cues. Notably, accumulating evidence indicate that the light-directed morphogenesis is profoundly affected by two recently identified phytochemicals, karrikins (KARs) and strigolactones (SLs). KARs and SLs are structurally related butenolides acting as signaling molecules during a variety of developmental steps, including seed germination. Their receptors and signaling mediators have been identified, and associated working mechanisms have been explored using gene-deficient mutants in various plant species. Of particular interests is that the KAR and SL signaling pathways play important roles in environmental responses, among which their linkages with photomorphogenesis are most comprehensively studied during seedling establishment. In this review, we focus on how the phytochemical and light signals converge on the optimization of morphogenic fitness. We also discuss molecular mechanisms underlying the signaling crosstalks with an aim of developing potential ways to improve crop productivity under climate changes."
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: Sompop Pinit, Lalichat Ariyakulkiat and Juthamas Chaiwanon.
Scientific Reports (2023)
Abstract: "Plant-derived smoke has been shown to promote plant growth and seed germination, but its roles and mechanisms in response to nutrient deficiency stress remain unclear. Plants respond to phosphorus (P) deficiency by undergoing morphological, physiological, and transcriptional changes in order to improve nutrient uptake efficiency. Here, we showed that rice straw-derived smoke water could promote root growth in rice (Oryza sativa cv. Nipponbare) grown under P-sufficient and P-deficient conditions. Transcriptome analysis of the root tissues identified 1309 genes up-regulated and 1311 genes down-regulated by smoke water under P-deficient conditions. The GO terms ‘glutathione transferase activity’ and ‘photosynthesis—light reaction’ were found to be significantly enriched among the genes that were up- and down-regulated by smoke water, respectively. Biochemical analysis showed that smoke water reduced P-deficient-induced accumulation of H2O2 and malondialdehyde (MDA), a lipid peroxidation marker, reduced sucrose contents, but increased Fe accumulation. Furthermore, smoke water suppressed the expression of strigolactone biosynthesis genes, which were strongly induced by P deficiency as an adaptive strategy to improve root P uptake. These results revealed a potential mechanism by which smoke water promotes root growth and interacts with P deficiency-induced transcriptional regulation to mitigate P deficiency stress in rice."
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: Peipei Xu, Jinbo Hu, Haiying Chen and Weiming Cai.
Cell Reports (2023)
Editor's view: Xu et al. show that KAR signaling protein SMAX1 inhibits seed germination under weak light conditions by regulating gibberellin (GA) biosynthesis. SMAX1 inhibits GA3ox2 gene expression and DELLA proteins interact with SMAX1 to regulate its transcriptional activity, indicating a crosstalk between KAR and GA signaling in regulating Arabidopsis seed germination.
Highlights • KAR signaling mutants have lower germination percentage under weak light • SMAX1 functions as an auto-regulated transcription factor • The interactions of SMAX1 with DELLA proteins regulate SMAX1 transcriptional activity • SMAX1 can inhibit the GA3ox2 gene expression, which is a key enzyme in GA biosynthesis
Abstract: "Karrikins (KARs) were first identified as a class of small-molecule chemicals derived from smoke that promote seed germination. However, the implied mechanism is still not well understood. Here, we find that KAR signaling mutants have a lower germination percentage than that of wild type under weak light conditions, and KARs promote seed germination through transcriptional activation of gibberellin (GA) biosynthesis via SMAX1. SMAX1 interacts with the DELLA proteins REPRESSOR of ga1-3-LIKE 1 (RGL1) and RGL3. The interaction enhances the transcriptional activity of SMAX1 and inhibits GIBBERELLIN 3-oxidase 2 (GA3ox2) gene expression. The KAR signaling mutant seed germination defect under weak light is partially rescued by exogenous application of GA3 or by GA3ox2 overexpression, and the rgl1 rgl3 smax1 triple mutant exhibits higher germination rates under weak light than the smax1 mutant. Thus, we show a crosstalk between KAR and GA signaling pathways via a SMAX1-DELLA module in regulating seed germination in Arabidopsis."
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: Sarika Singh, Moin Uddin, M. Masroor A. Khan, Aman Sobia Chishti, Sangram Singh and Urooj Hassan Bhat.
Plant Stress (2023)
Highlights: • Smoke and its active ingredients promote seed germination, seedling growth and mitigation of abiotic stresses. • Plant-derived smoke and karrikin maintain oxidative equilibrium by controlling the cell's antioxidant apparatus. • Plant derived smoke and karrikin interacts with phytohormones to reduce the oxidative damage, drought, and heavy metal stress.
Abstract: "Plant-derived smoke has the potential to be used in tissue culture, agriculture, and ecological restoration. Karrikin is an active constituent of plant-derived smoke and a strong germination stimulant. Karrikin and strigolactone share comparable signaling pathways and exhibit structural similarities. Smoke and its active ingredients promote seed germination as well as other physiological activities, such as seedling growth and abiotic stress mitigation. Additionally, plant-derived smoke and karrikin maintain oxidative equilibrium by controlling the cell's antioxidant machinery. In order to reduce abiotic challenges such oxidative damage, drought, and heavy metal stress, plant derived smoke as well as karrikin interacts with a number of phytohormones. Various genomics studies have been progressed in revealing the mechanism of action of plant derived smoke and karrikin in mitigation of abiotic stresses in plants. This review article focuses on the role of plant-derived smoke and karrikinolide in improving stress tolerance."
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."
|
