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1. Transcriptional regulation of development by SMAX1-LIKE proteins – targets of strigolactone and karrikin/KAI2 ligand signaling

   https://doi.org/10.1093/jxb/eraf027  

   Chang, Sun Hyun; George, Wesley; Nelson, David C (January 2025, Journal of Experimental Botany)

   Best, Norman (Ed.)

   Abstract SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE (SMXL) proteins comprise a family of plant growth regulators that includes downstream targets of the karrikin (KAR)/KAI2 ligand (KL) and strigolactone (SL) signaling pathways. Following the perception of KAR/KL or SL signals by α/β hydrolases, some types of SMXL proteins are polyubiquitinated by an E3 ubiquitin ligase complex containing the F-box protein MORE AXILLARY GROWTH2 (MAX2)/DWARF3 (D3), and proteolyzed. Because SMXL proteins interact with TOPLESS (TPL) and TPL-related (TPR) transcriptional co-repressors, SMXL degradation initiates changes in gene expression. This simplified model of SMXL regulation and function in plants must now be revised in light of recent discoveries. It has become apparent that SMXL abundance is not regulated by KAR/KL or SL alone, and that some SMXL proteins are not regulated by MAX2/D3 at all. Therefore, SMXL proteins should be considered as signaling hubs that integrate multiple cues. Here we review the current knowledge of how SMXL proteins impose transcriptional regulation of plant development and environmental responses. SMXL proteins can bind DNA directly and interact with transcriptional regulators from several protein families. Multiple mechanisms of downstream genetic control by SMXL proteins have been identified recently that do not involve the recruitment of TPL/TPR, expanding the paradigm of SMXL function. 

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2. KARRIKIN UP-REGULATED F-BOX 1 (KUF1) imposes negative feedback regulation of karrikin and KAI2 ligand metabolism in Arabidopsis thaliana

   https://doi.org/10.1073/pnas.2112820119  

   Sepulveda, Claudia; Guzmán, Michael A.; Li, Qingtian; Villaécija-Aguilar, José Antonio; Martinez, Stephanie E.; Kamran, Muhammad; Khosla, Aashima; Liu, Wei; Gendron, Joshua M.; Gutjahr, Caroline; et al (March 2022, Proceedings of the National Academy of Sciences)

   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 KAR 1 , 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 KAR 1 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). 

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3. Strigolactones: diversity, perception, and hydrolysis

   https://doi.org/10.1007/s11101-023-09853-4  

   Guercio, Angelica M.; Palayam, Malathy; Shabek, Nitzan (January 2023, Phytochemistry Reviews)

   Strigolactones (SLs) are a unique and novel class of phytohormones that regulate numerous processes of growth and development in plants. Besides their endogenous functions as hormones, SLs are exuded by plant roots to stimulate critical interactions with symbiotic fungi but can also be exploited by parasitic plants to trigger their seed germination. In the past decade, since their discovery as phytohormones, rapid progress has been made in understanding the SL biosynthesis and signaling pathway. Of particular interest are the diversification of natural SLs and their exact mode of perception, selectivity, and hydrolysis by their dedicated receptors in plants. Here we provide an overview of the emerging field of SL perception with a focus on the diversity of canonical, non-canonical, and synthetic SL probes. Moreover, this review offers useful structural insights into SL perception, the precise molecular adaptations that define receptor-ligand specificities, and the mechanisms of SL hydrolysis and its attenuation by downstream signaling components. 

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4. Dominant-Negative KAI2d Paralogs Putatively Attenuate Strigolactone Responses in Root Parasitic Plants

   https://doi.org/10.1093/pcp/pcae106  

   White, Alexandra_R F; Kane, Annalise; Ogawa, Satoshi; Shirasu, Ken; Nelson, David C (September 2024, Plant And Cell Physiology)

   Abstract Many root parasitic plants in the Orobanchaceae use host-derived strigolactones (SLs) as germination cues. This adaptation facilitates attachment to a host and is particularly important for the success of obligate parasitic weeds that cause substantial crop losses globally. Parasite seeds sense SLs through ‘divergent’ KARRIKIN INSENSITIVE2 (KAI2d)/HYPOSENSITIVE TO LIGHT α/β-hydrolases that have undergone substantial duplication and diversification in Orobanchaceae genomes. After germination, chemotropic growth of parasite roots toward a SL source also occurs in some species. We investigated which of the seven KAI2d genes found in a facultative hemiparasite, Phtheirospermum japonicum, may enable chemotropic responses to SLs. To do so, we developed a triple mutant Nbd14a,b kai2i line of Nicotiana benthamiana in which SL-induced degradation of SUPPRESSOR OF MORE AXILLARY GROWTH2 (MAX2) 1 (SMAX1), an immediate downstream target of KAI2 signaling, is disrupted. In combination with a transiently expressed, ratiometric reporter of SMAX1 protein abundance, this mutant forms a system for the functional analysis of parasite KAI2d proteins in a plant cellular context. Using this system, we unexpectedly found three PjKAI2d proteins that do not trigger SMAX1 degradation in the presence of SLs. Instead, these PjKAI2d proteins inhibit the perception of low SL concentrations by SL-responsive PjKAI2d in a dominant-negative manner that depends upon an active catalytic triad. Similar dominant-negative KAI2d paralogs were identified in an obligate hemiparasitic weed, Striga hermonthica. These proteins suggest a mechanism for attenuating SL signaling in parasites, which might be used to enhance the perception of shallow SL gradients during root growth toward a host or to restrict germination responses to specific SLs. 

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5. Not so hidden anymore: Advances and challenges in understanding root growth under water deficits

   https://doi.org/10.1093/plcell/koae055  

   Voothuluru, Priya; Wu, Yajun; Sharp, Robert E (February 2024, The Plant Cell)

   Abstract Limited water availability is a major environmental factor constraining plant development and crop yields. One of the prominent adaptations of plants to water deficits is the maintenance of root growth that enables sustained access to soil water. Despite early recognition of the adaptive significance of root growth maintenance under water deficits, progress in understanding has been hampered by the inherent complexity of root systems and their interactions with the soil environment. We highlight selected milestones in the understanding of root growth responses to water deficits, with emphasis on founding studies that have shaped current knowledge and set the stage for further investigation. We revisit the concept of integrated biophysical and metabolic regulation of plant growth and use this framework to review central growth-regulatory processes occurring within root growth zones under water stress at subcellular to organ scales. Key topics include the primary processes of modifications of cell wall–yielding properties and osmotic adjustment, as well as regulatory roles of abscisic acid and its interactions with other hormones. We include consideration of long-recognized responses for which detailed mechanistic understanding has been elusive until recently, for example hydrotropism, and identify gaps in knowledge, ongoing challenges, and opportunities for future research. 

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