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Authors: María Isabel Puga, César Poza-Carrión, Iris Martinez-Hevia, Laura Perez-Liens and Javier Paz-Ares
Journal of Plant Research (2024)
Abstract: "Phosphorus is indispensable for plant growth and development, with its status crucial for determining crop productivity. Plants have evolved various biochemical, morphological, and developmental responses to thrive under conditions of low P availability, as inorganic phosphate (Pi), the primary form of P uptake, is often insoluble in soils. Over the past 25 years, extensive research has focused on understanding these responses, collectively forming the Pi starvation response system. This effort has not only expanded our knowledge of strategies to cope with Pi starvation (PS) but also confirmed their adaptive significance. Moreover, it has identified and characterized numerous components of the intricate regulatory network governing P homeostasis. This review emphasizes recent advances in PS signaling, particularly highlighting the physiological importance of local PS signaling in inhibiting primary root growth and uncovering the role of TORC1 signaling in this process. Additionally, advancements in understanding shoot-root Pi allocation and a novel technique for studying Pi distribution in plants are discussed. Furthermore, emerging data on the regulation of plant-microorganism interactions by the PS regulatory system, crosstalk between the signaling pathways of phosphate starvation, phytohormones and immunity, and recent studies on natural variation in Pi homeostasis are addressed.
Authors: Huwei Sun, Hanyun Wang and Chengcai Chu.
Science China - Life Sciences (2024)
Excerpt: "An earlier study has demonstrated that SL biosynthesis requires the symbiotic GRAS type transcription factors NODULATION SIGNALING PATHWAY 1 NSP1 and NSP2 in Medicago truncatula and rice (Liu et al., 2011). Very recently, Yuan et al. (2023) revealed the upstream transcription factors of SL bio synthesis and the molecular mechanism by which SLs regulate N-P balance in response to LP. Under LP conditions, the central P signaling regulator PHOSPHATE STARVATION RESPONSE (OsPHR2) directly activated the expression of NSP1, NSP2, and SL biosynthesis genes D27, D17 and Os900 in rice. NSP1 and NSP2 further formed heterodimers and activated the expression of SL biosynthesis genes (D27, D17, D10, Os900 and Os1400), leading to elevated SL s levels in rice roots and root exudates under Pi deficient conditions . Moreover, the SLs levels in nsp1, nsp2 and nsp1 nsp2 double mutants under LP were similar to or only several fold those in WT plants under high P (HP) conditions, demonstrating that NSP1 and NSP2 are essential for SL biosynthesis under LP conditions. SLs further activated their signaling pathways, promoting the expression of the tillering suppressor TEOSINTE BRANCHED 1 (OsTB1) and thus reducing tiller numbers. To elucidate the mechanisms by which SLs regulate root development and nutrient absorption, Yuan et al. (2023) identified the early SL responsive genes in rice roots using the SL synthetic analogs GR24 4DO and GR24 5DS , which specifically activated the SL signaling pathway. Based on the RNA seq results, the authors identified 150 upregulated genes and 168 downregulated genes, which were commonly regulated by both GR24 and LP treatments. Among the genes repressed by GR24 and LP supply, CROWN ROOTLESS 1 (CRL1)/ADVENTITIOUS ROOTLESS 1 (ARL1) was a newly identified early SL responsive gene. And its expression was inhibited by the activation of the NSP1/2 SL signaling pathway, leading to a reduction in lateral root density of rice under LP conditions (Figure 1)."
Authors: Guan-Ting Erica Chen, Jian You Wang, Cristina Votta, Justine Braguy, Muhammad Jamil, Gwendolyn K. Kirschner, Valentina Fiorilli, Lamis Berqdar, Aparna Balakrishna, Ikram Blilou, Luisa Lanfranco and Salim Al-Babili.
PNAS (2023)
Significance: Strigolactones (SLs) are multifunctional, structurally diverse secondary metabolites fulfilling the function of a hormone. Whether a particular SL exerts specific functions is one of the most important questions in SL biology. Here, we generated and characterized rice mutants lacking the common SLs 4-deoxyorobanchol and/or its derivative orobanchol, which represent one of the two SL subfamilies, i.e., canonical SLs. We show that 4-deoxyorobanchol is not a determinant of shoot branching, but has a specific function as a regulator of shoot, root, and panicle growth. Accumulation of 4-deoxyorobanchol affects auxin homeostasis and negatively impacts the symbiosis with mycorrhizal fungi. Our data reveal specific hormonal functions of canonical SLs and pave the way for targeted modulation of rice architecture and rhizospheric interactions.
Abstract: "Strigolactones (SLs) regulate many developmental processes, including shoot-branching/tillering, and mediate rhizospheric interactions. SLs originate from carlactone (CL) and are structurally diverse, divided into a canonical and a noncanonical subfamily. Rice contains two canonical SLs, 4-deoxyorobanchol (4DO) and orobanchol (Oro), which are common in different plant species. The cytochrome P450 OsMAX1-900 forms 4DO from CL through repeated oxygenation and ring closure, while the homologous enzyme OsMAX1-1400 hydroxylates 4DO into Oro. To better understand the biological function of 4DO and Oro, we generated CRISPR/Cas9 mutants disrupted in OsMAX1-1400 or in both OsMAX1-900 and OsMAX1-1400. The loss of OsMAX1-1400 activity led to a complete lack of Oro and an accumulation of its precursor 4DO. Moreover, Os1400 mutants showed shorter plant height, panicle and panicle base length, but no tillering phenotype. Hormone quantification and transcriptome analysis of Os1400 mutants revealed elevated auxin levels and changes in the expression of auxin-related, as well as of SL biosynthetic genes. Interestingly, the Os900/1400 double mutant lacking both Oro and 4DO did not show the observed Os1400 architectural phenotypes, indicating their being a result of 4DO accumulation. Treatment of wild-type plants with 4DO confirmed this assumption. A comparison of the Striga seed germinating activity and the mycorrhization of Os900, Os900/1400, and Os1400 loss-of-function mutants demonstrated that the germination activity positively correlates with 4DO content while disrupting OsMAX1-1400 has a negative impact on mycorrhizal symbiosis. Taken together, our paper deciphers the biological function of canonical SLs in rice and reveals their particular contributions to establishing architecture and rhizospheric communications."
Authors: Vincent Lailheugue, Isabelle Merlin, Stéphanie Boutet, François Perreau, Jean-Bernard Pouvreau, Sabine Delgrange, Paul-Henri Ducrot, Betty Cottyn-Boitte, Gregory Mouille and Virginie Lauvergeat.
Phytochemistry (2023)
Highlights • Non-canonical Strigolactone compounds were identified in root exudates of grapevine rootstocks • Nitrogen deprivation increases exudation strigolactone compounds in grapevine rootstocks. • Vitislactone showed an original non-canonical feature. • Heliolactone-like compound was found only in exudates of Vitis riparia Gloire de Montpellier rootstock.
Abstract: "Strigolactones are compounds produced by plant roots in response to nutrient deficiency, acting both as local and systemic signals to control development and nutrition. Strigolactones are exuded in the rhizosphere to positively influence interactions with beneficial microbes. LC-MS/MS analysis shows that two genetically distinct grapevine rootstocks exudate one or two non-canonical strigolactones when subjected to low nitrogen conditions. Gene expression profiles and orobanche seed germination assays confirm that the biosynthesis and exudation of non-canonical compounds is the preferred pathway. The first compound, corresponding to heliolactone or 6-epi-heliolactone, is only exuded by the rootstock showing lower shoot branching and a higher level of mycorrhization with arbuscular mycorrhizal fungi. The structure of the second compound exuded by both rootstocks was identified by NMR and LC-MS/MS analysis. It is a non-canonical strigolactone, which has never been identified in another species. This first identification of a natural compound with the potential to stimulate beneficial root-microbe interactions in grapevines opens new perspectives in viticulture."
Authors: Muhammad Jamil, Pei-Yu Lin, Lamis Berqdar, Jian You Wang, Ikuo Takahashi, Tsuyoshi Ota, Noor Alhammad, Guan-Ting Erica Chen, Tadao Asami and Salim Al-Babili.
Biomolecules (2023)
Abstract: "The apocarotenoid zaxinone is a recently discovered regulatory metabolite required for proper rice growth and development. In addition, zaxinone and its two mimics (MiZax3 and MiZax5) were shown to have a remarkable growth-promoting activity on crops and a capability to reduce infestation by the root parasitic plant Striga through decreasing strigolactone (SL) production, suggesting their potential for application in agriculture and horticulture. In the present study, we developed a new series of MiZax via structural modification of the two potent zaxinone mimics (MiZax3 and MiZax5) and evaluated their effect on plant growth and Striga infestation. In general, the structural modifications to MiZax3 and MiZax5 did not additionally improve their overall performance but caused an increase in certain activities. In conclusion, MiZax5 and especially MiZax3 remain the likely most efficient zaxinone mimics for controlling Striga infestation."
Authors: Qian Wang, Ping Yang, Theivanayagam Maharajan, Muthusamy Ramakrishnan, Muhammad Asim, Renyi Gui and Mingbing Zhou.
Journal of Agricultural and Food Chemistry (2023)
Abstract: "Both phosphate (Pi) deficiency and high Pi significantly affect moso bamboo growth and degrade bamboo forests. A novel plant hormone, strigolactone (SL), plays a crucial role in root growth under low Pi, but the SL regulatory mechanism has not been systematically reported in moso bamboo. In our study, we investigated the SL-mediated root growth mechanism in response to Pi stress in moso bamboo. With the decrease of the Pi level, 5-deoxystrigol and strigol significantly increased in the root exudates. Transcriptome sequencing of the primary root tip and lateral root primordium zone (LRP) under low, sufficient, and high Pi indicated that SL-biosynthesis and -signaling changes are part of the early root responses. The effects of the SL analogue (rac-GR24) and SL inhibitor (TIS108) on the root architecture under low and high Pi revealed that SL mediates bamboo root responses by regulating its biosynthesis and signal transduction and influencing other hormone pathways."
Authors: Jian You Wang, Justine Braguy and Salim Al-Babili.
Pant Signaling & Behavior (2023)
Abstract: "The cleavage of plant carotenoids leads to apocarotenoids, a group of metabolites including precursors of the hormones strigolactones (SLs) and abscisic acid, regulatory and signaling molecules. Zaxinone is a recently discovered apocarotenoid growth regulator that improves growth and suppress SL biosynthesis in rice (Oryza sativa). To test if zaxinone also counteracts the growth regulatory effects of SLs in rice, we co-supplied zaxinone and the synthetic SL analog rac-GR24 to the rice SL-deficient DWARF17 (d17) mutant. Results showed that co-application of GR24 and zaxinone still rescued d17 phenotype, indicating that zaxinone and GR24 act independently in regulating root and shoot growth and development in rice."
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: Songtao Jiu, Yan Xu, Jiyuan Wang, Muhammad Salman Haider, Jieming Xu, Lei Wang, Shiping Wang, Jiajia Li, Xunju Liu, Wanxia Sun, Wenping Xu and Caixi Zhang.
Scientia Horticulturae (2022)
Highlights: • Strigolactones (SLs) markedly affected the root growth and development in grapevine. • SLs remarkably altered the endogenous hormones levels of grapevine roots. • Several DEGs related to hormones, root development, and cell-cycle induction pathways were identified.
Abstract: "Strigolactones (SLs) are vital rhizosphere signals that act as phytohormones modulating plant root growth and development. After treatment for 12 days, the synthetic SLs analog GR24 significantly increased the number and density of fine root. The data indicated that different concentrations of GR24 exerted opposite effects on lateral root (LR) initiation. High concentration (10 μM) of GR24, similar to 10 μM TIS108 (a triazole-type inhibitor of SLs), acted as a positive regulator for LR initiation, whereas the treatment with a low concentration (0.1 μM) of GR24 markedly reduced LR density. In addition, root length and surface area were markedly increased by the treatment with 10 μΜ GR24, compared with those of the controls. In root samples treated with 0.1 μM GR24, 10 μM GR24, and 10 μM TIS108, 4534, 5022, and 3803 differentially expressed genes (DEGs) were identified compared to the control, respectively. The results of RNA-Seq highlighted several DEGs, such as ARF, EBF, ERF, CYCA1, and LOB, which play critical roles in hormone signaling, cell cycle, and root growth and development in grapevines. UPLC-MS analysis further demonstrated that SLs application remarkably altered the levels of endogenous hormones. In particular, indole-3-acetic acid (IAA) content in grapevine roots treated with 10 μΜ TIS108 was approximately 4.78 times higher than that in the control, whereas it was the opposite following the 0.1 μΜ or 10 μΜ GR24 treatment. Our study provides the first comprehensive description of the effect of SLs on grapevine root development caused by interacting with other phytohormone signaling, and lays a solid theoretical basis for using SLs to regulate root growth and development in grapevines."
Authors: Yanting Wang, Hernando G. Suárez Duran, Jan C. van Haarst, Elio G.W.M Schijlen, Carolien Ruyter-Spira, Marnix H. Medema, Lemeng Dong and Harro J. Bouwmeester.
BMC Plant Biology (2021)
Abstract: "Background - Phosphorus (P) is an essential macronutrient for plant growth and development. Upon P shortage, plant responds with massive reprogramming of transcription, the Phosphate Starvation Response (PSR). In parallel, the production of strigolactones (SLs)—a class of plant hormones that regulates plant development and rhizosphere signaling molecules—increases. It is unclear, however, what the functional link is between these two processes. In this study, using tomato as a model, RNAseq was used to evaluate the time-resolved changes in gene expression in the roots upon P starvation and, using a tomato CAROTENOID CLEAVAGE DIOXYGENASES 8 (CCD8) RNAi line, what the role of SLs is in this. Results - Gene ontology (GO)-term enrichment and KEGG analysis of the genes regulated by P starvation and P replenishment revealed that metabolism is an important component of the P starvation response that is aimed at P homeostasis, with large changes occurring in glyco-and galactolipid and carbohydrate metabolism, biosynthesis of secondary metabolites, including terpenoids and polyketides, glycan biosynthesis and metabolism, and amino acid metabolism. In the CCD8 RNAi line about 96% of the PSR genes was less affected than in wild-type (WT) tomato. For example, phospholipid biosynthesis was suppressed by P starvation, while the degradation of phospholipids and biosynthesis of substitute lipids such as sulfolipids and galactolipids were induced by P starvation. Around two thirds of the corresponding transcriptional changes depend on the presence of SLs. Other biosynthesis pathways are also reprogrammed under P starvation, such as phenylpropanoid and carotenoid biosynthesis, pantothenate and CoA, lysine and alkaloids, and this also partially depends on SLs. Additionally, some plant hormone biosynthetic pathways were affected by P starvation and also here, SLs are required for many of the changes (more than two thirds for Gibberellins and around one third for Abscisic acid) in the gene expression. Conclusions - Our analysis shows that SLs are not just the end product of the PSR in plants (the signals secreted by plants into the rhizosphere), but also play a major role in the regulation of the PSR (as plant hormone)."
Authors: Mohammad Golam Mostofa, Md. Mezanur Rahman, Kien Huu Nguyen, Weiqiang Li, Yasuko Watanabe, Cuong Duy Tran, Minghui Zhang, Misao Itouga, Masayuki Fujita, Lam-Son Phan Tran.
Journal of Hazardous Materials (2021)
Highlights: • Strigolactones (SLs)’ mechanisms underpinning arsenic-stress tolerance in rice are unknown. • SL-deficient d10 and d17 rice mutants accumulated higher amount of arsenic in roots than WT. • SL deficiency increased oxidative stress and membrane damage in arsenate-treated d10 and d17 roots. • SL-functions in arsenate-stress tolerance are linked to GSH-assisted vacuolar-sequestration of arsenic in roots. • WT roots maintained better redox status and antioxidant system than d10 and d17 roots under arsenate-stress.
Abstract: "We explored genetic evidence for strigolactones’ role in rice tolerance to arsenate-stress. Comparative analyses of roots of wild-type (WT) and strigolactone-deficient mutants d10 and d17 in response to sodium arsenate (Na2AsO4) revealed differential growth inhibition [WT (11.28%) vs. d10 (19.76%) and d17 (18.03%)], biomass reduction [(WT (33.65%) vs. d10 (74.86%) and d17 (60.65%)] and membrane damage (WT < d10 and d17) at 250 μM Na2AsO4. Microscopic and biochemical analyses showed that roots of WT accumulated lower levels of arsenic and oxidative stress indicators like reactive oxygen species, malondialdehyde and hydrogen peroxide than those of strigolactone-deficient mutants. qRT-PCR data indicated lower expression levels of genes (OsPT1, OsPT2, OsPT4 and OsPT8) encoding phosphate-transporters in WT roots than mutant roots, explaining the decreased arsenate and phosphate uptake by WT roots. Increased levels of glutathione and OsPCS1 and OsABCC1 transcripts indicated an efficient vacuolar-sequestration of arsenic in WT roots. Furthermore, higher activities (transcript levels) of SOD (OsCuZnSOD1 and OsCuZnSOD2), APX (OsAPX1 and OsAPX2) and CAT (OsCATA) corresponded to lower oxidative damage in WT roots compared with strigolactone-mutant roots. Collectively, these results highlight that strigolactones are involved in arsenic-stress mitigation by regulating arsenate-uptake, glutathione-biosynthesis, vacuolar-sequestration of arsenic and antioxidant defense responses in rice roots."
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Authors: Jian You Wang, Guan-Ting Erica Chen, Justine Braguy and Salim Al-Babili.
Trends in Plant Science (2024)
Highlights: Strigolactones (SLs) are structurally diverse and divided into canonical and non-canonical subgroups. SLs are generally considered as plant hormones, best known for inhibiting shoot branching/tillering. SLs are rhizospheric signals important for arbuscular mycorrhizal symbiosis, which may be their ancestral function that is conserved from liverworts to flowering plants. Recent results have revealed functional specificity, indicating that canonical SLs are not the tillering/branching inhibitory hormone in rice or tomato. Increasing the content of 4-deoxyorobanchol in rice by interrupting its hydroxylation affects root, shoot, and panicle growth, suggesting that this canonical SL has hormonal functions. Reducing the levels of canonical SLs by genome editing or applying specific inhibitors is a promising strategy for reducing Striga parasitism.
Abstract: "Strigolactones (SLs) act as regulators of plant architecture as well as signals in rhizospheric communications. Reduced availability of minerals, particularly phosphorus, leads to an increase in the formation and release of SLs that enable adaptation of root and shoot architecture to nutrient limitation and, simultaneously, attract arbuscular mycorrhizal fungi (AMF) for establishing beneficial symbiosis. Based on their chemical structure, SLs are designated as either canonical or non-canonical; however, the question of whether the two classes are also distinguished in their biological functions remained largely elusive until recently. In this review we summarize the latest advances in SL biosynthesis and highlight new findings pointing to rhizospheric signaling as the major function of canonical SLs."
Authors: Abdugaffor Ablazov, Muhammad Jamil, Imran Haider, Jian You Wang, Vanessa Melino, Moez Maghrebi, Gianpiero Vigani, Kit Xi Liew, Pei-Yu Lin, Guan-Ting Chen, Hendrik NJ Kuijer, Lamis Berqdar, Teresa Mazzarella, Valentina Fiorilli, Luisa Lanfranco, Xiongjie Zheng, Nai-Chiang Dai, Ming-Hsin Lai, Yue-Ie Caroline Hsing, Mark Tester, Ikram Blilou and Salim Al-Babili.
bioRxiv (2023)
Abstract: "The rice Zaxinone Synthase (ZAS) gene encodes a carotenoid cleavage dioxygenase (CCD) that forms the apocarotenoid growth regulator zaxinone. Here, we generated and characterized constitutive ZAS-overexpressing rice lines, to better understand ZAS role in determining zaxinone content and regulating growth and architecture. ZAS overexpression enhanced endogenous zaxinone level, promoted root growth and meristem size, and increased the number of productive tillers, leading to an up to 30% higher grain yield per plant. Hormone analysis revealed a decrease in strigolactone (SL) content, which we confirmed by rescuing the high-tillering phenotype through application of a SL analog. Metabolomics analysis revealed that ZAS overexpressing plants accumulate higher amounts of monosaccharide sugars, in line with transcriptome analysis. Moreover, transgenic plants showed higher carbon (C) assimilation rate and elevated root phosphate, nitrate and sulfate level, enhancing the tolerance towards low phosphate (Pi) and indicating a generally better nutrient uptake. Our study shows that ZAS regulates hormone homeostasis and a combination of physiological processes to promote growth and grain yield, which makes this gene an excellent candidate for sustainable crop improvement."
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: Zhaoyong Kang, Yujie Yan, Ruirui Lu, Xiaoqi Dong, Jun Xu, Dong Zheng, Suhua Li, Qingzhi Gao and Shengnan Liu.
Journal of Agricultural and Food Chemistry (2023)
Abstract: "The artificially synthesized strigolactone (SL) analogue GR24 is currently the most widely used reference compound in studying the biological functions of SLs. To elucidate the structure–activity relationship and find more promising derivatives with unique molecular profiles, we design and synthesized three series of novel GR24 derivatives and explored their activities in hypocotyl and root development of Arabidopsis. Among the 50 synthesized compounds, A11a, A12a, and A20d were found to have high activities comparable to GR24 for hypocotyl and/or primary root elongation inhibition in Arabidopsis. Some new analogues have been discovered to exhibit unique activities: (1) A20c, A21e, and A21o are specific inhibitors in primary root elongation; (2) A21c, A26c, and A27a exhibit a high promotion effect on Arabidopsis primary root elongation; and (3) A27e possesses the most unique profiles completely opposite to GR24 that promotes both hypocotyl elongation and primary root development. Moreover, we revealed that the AtD14 receptor does not affect the inhibitory effect of SL analogues in Arabidopsis root development. The ligand–receptor interactions for the most representative analogues A11a and A27e were deciphered with a long time scale molecular dynamics simulation study, which provides the molecular basis of their distinct functions, and may help scientists design novel phytohormones.
Authors: Muhammad Jamil, Yagiz Alagoz, Jian You Wang, Guan-Ting Erica Chen , Lamis Berqdar, Najeh M. Kharbatia, Juan C. Moreno, Hendrik N. J. Kuijer and Salim Al-Babili.
bioRxiv (2023)
Abstract: "Seeds of the root parasitic plant Striga hermonthica undergo a conditioning process under humid and warm environments before germinating in response to host-released stimulants, particularly strigolactones (SLs). The plant hormone abscisic acid (ABA) regulates different growth and developmental processes, and stress response; however, its role during Striga seed germination and early interactions with host plants is under-investigated. Here, we show that ABA inhibited Striga seed germination and that hindering its biosynthesis induced conditioning and germination in unconditioned seeds, which was significantly enhanced by treatment with the SL analog rac-GR24. However, the inhibitory effect of ABA remarkably decreased during conditioning, confirming the loss of sensitivity towards ABA in later developmental stages. ABA measurement showed a significant reduction of its content during the early conditioning stage and a significant increase upon rac-GR24-triggered germination. We observed this increase also in released seed exudates, which was further confirmed by using the Arabidopsis ABA-reporter GUS marker line. Seed exudates of germinated seeds, containing elevated levels of ABA, impaired the germination of surrounding Striga seeds in vitro and promoted root growth of a rice host towards germinated Striga seeds. Application of ABA as a positive control caused similar effects, indicating its function in Striga/Striga and Striga/host communications. In summary, we show that ABA is an essential player during seed dormancy and germination processes in Striga and acts as a rhizospheric signal released by germinated parasitic seeds to provide a competitive advantage and support host infestation."
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: Runming Zhang, Yanlong Dong, Yuanyuan Li, Guangyue Ren, Chao Chen and Xiaoxia Jin.
Gene (2023)
Highlights: • The over-expression of SLs signaling pathway gene CsMAX2 increased the tolerance to salt, drought and ABA stress of Arabidopsis thaliana L. • CsMAX2 might improve plant tolerance by regulating the expression of stress related genes, ABA signaling pathway and SLs related genes. • The stress tolerance induced by CsMAX2 might be related to ABA, and it preliminary concluded that there was partially correlation between SLs and ABA.
Abstract: "Recent studies have demonstrated that strigolactones (SLs) participate in the regulation of stress adaptation, however, the mechanisms remain elusive. MAX2 (MORE AXILLARY GROWTH2) is the key gene in the signal transduction pathway of SLs. This study aimed to clone and functionally characterize the CsMAX2 gene of cucumber in Arabidopsis. The results showed that the expression levels of the CsMAX2 gene changed significantly after salt, drought, and ABA stresses in cucumber. Moreover, the overexpression of CsMAX2 promoted stress tolerance and increased the germination rate and root length of Arabidopsis thaliana. Meanwhile, the content of chlorophyll increased and malondialdehyde decreased in CsMAX2 OE lines under salt and drought stresses. Additionally, the expression levels of stress-related marker genes, especially AREB1 and COR15A, were significantly upregulated under salt stress, while the expression levels of all genes were upregulated under drought stress, except ABI4 and ABI5 genes. The level of NCED3 continued to rise under both salt and drought stresses. In addition, D10 and D27 gene expression level also showed a continuous increase under ABA stress. The result suggested the interaction between SL and ABA in the process of adapting to stress. Overall, CsMAX2 could positively regulate salt, drought, and ABA stress resistance, and this process correlated with ABA transduction."
Authors: Huwei Sun, Weiqiang Li, David J. Burritt, Hongtao Tian, Heng Zhang, Xiaohan Liang, Yuchen Miao, Mohammad Golam Mostofa and Lam-Son Phan Tran.
The Crop Journal (2022)
Abstract: "Strigolactones (SLs), which are biosynthesized mainly in roots, modulate various aspects of plant growth and development. Here, we review recent research on the role of SLs and their cross-regulation with auxin, cytokinin, and ethylene in the modulation of root growth and development. Under nutrient-sufficient conditions, SLs regulate the elongation of primary roots and inhibit adventitious root formation in eudicot plants. SLs promote the elongation of seminal roots and increase the number of adventitious roots in grass plants in the short term, while inhibiting lateral root development in both grass and eudicot plants. The effects of SLs on the elongation of root hairs are variable and depend on plant species, growth conditions, and SL concentration. Nitrogen or phosphate deficiency induces the accumulation of endogenous SLs, modulates root growth and development. Genetic analyses indicate cross-regulation of SLs with auxin, cytokinin, and ethylene in regulation of root growth and development. We discuss the implications of these studies and consider their potential for exploiting the components of SL signaling for the design of crop plants with more efficient soil-resource utilization."
Authors: Songtao Jiu, Yan Xu, Xingnan Xie, Jiyuan Wang, Jieming Xu, Xunju Liu, Wanxia Sun, Wenping Xu, Shiping Wang and Caixi Zhang.
Environmental and Experimental Botany (2022)
Highlights: • Strigolactones (SLs) markedly affected the root architecture of cherry rootstock. • SLs remarkably altered the endogenous hormones levels of cherry rootstock roots. • X-ray micro-CT scanning is an effective method for non-destructive observation of roots. • Several DEGs related to hormones, root development, and cell-cycle induction pathways were identified.
Abstract: "Strigolactones (SLs) are new phytohormones that modulate the growth and development of plant roots. Rootstocks affect horticulturally important traits of cultivars, including tree size, abiotic stress tolerance, and disease resistance. This study focused on understanding the effects of SLs on transcriptional regulation and root system architecture of cherry rootstock. Here, we examined the morphology and also profiled endogenous hormones levels, and transcript levels of key genes from the roots treated with synthetic SLs analog GR24 or SLs inhibitor TIS108. Cherry rootstock plantlets treated with 10 μM TIS108 exhibited fewer adventitious root (AR). The diameter of AR at 5, 10, and 30 days after 0.1 μM GR24 treatment decreased by 23.8, 23.2 and 11.5%, respectively, whereas AR diameter was 1.15, 1.15, and 1.16 times more than that in the control when 10 μM TIS108 applied, respectively. LR number in plantlets treated with 10 μM TIS108 reached the maximum of 11.25 for each AR, much higher than those of the control and other treatments at 30 days after treatment (DAT). X-ray micro-CT scanning also showed that 10 μM TIS108 markedly induced LR initiation, but suppressed LR elongation. Furthermore, 2946, 1536, and 2146 differentially expressed genes (p-value < 0.05, |log2Fold Change|> 1) were identified in the root samples treated with 0.1 μM GR24, 10 μM GR24, and 10 μM TIS108, respectively, compared to the control. RNA-Seq findings highlighted several DEGs, such as ARF, PP2C, ERF, LOB, and CYC, which play critical roles in hormone signaling, cell cycle, and root growth and development. An UPLC-MS analysis further demonstrated that SLs remarkably altered the levels of endogenous hormones in cherry rootstock. In particular, the content of endogenous indole-3-acetic acid (IAA) markedly increased by 64.6, 52.1 and 173.5% after treatment with 0.1 μM GR24, 10 μM GR24, and 10 μM TIS108, respectively. Overall, our study indicated that SLs affected root system architecture by interacting with other plant hormones, which will provide a solid theoretical basis for the effects of SLs on the root system architecture of other woody plants."
Authors: Michio Kuruma, Taiki Suzuki and Yoshiya Seto.
Bioorganic & Medicinal Chemistry Letters (2021)
Abstract: "Root parasitic plant germination is induced by the host-derived chemical, strigolactone (SL). We found that a major microbial culture broth component, tryptone, inhibits the SL-inducible germination of a root parasitic plant, Orobanche minor. l-tryptophan (l-Trp) was isolated as the active compound from tryptone. We further found that l-Trp related compounds (1b-11), such as a major plant hormone auxin (8, indole-3-acetic acid; IAA), also inhibit the germination and post-radicle growth of O. minor. We designed a hybrid chemical (13), in which IAA is attached to a part of SL, and found that this synthetic analog induced the germination of O. minor, and also inhibited post-radicle growth. Moreover, contrary to our expectations, we found that N-acetyl Trp (9) showed germination stimulating activity, and introduction of a substitution at C-5 position increased its activity (12a-12f). Our data, in particular, the discovery of a structurally hybrid compound that has two activities that induce spontaneous germination and inhibit subsequent radical growth, would provide new types of germination regulators for root parasitic plants."
Authors: Huwei Sun, Xiaoli Guo, Xuejiao Qi, Fan Feng, Xiaonan Xie, Yali Zhang and Quanzhi Zhao.
The Plant Journal (2021)
Abstract: "Nitrogen (N) is an essential major nutrient for food crops. Although ammonium (NH4+) is the primary N source of rice, nitrate (NO3‐) can also be absorbed and utilized. Rice responds to NO3‐ application by altering its root morphology, such as root elongation. Strigolactones (SLs) are important modulators of root length. However, the roles of SLs and their downstream genes in NO3‐‐induced root elongation remain unclear. Here, the levels of total N and SL (4‐deoxyorobanchol), and the responses of seminal root (SR) lengths to NH4+ and NO3‐ were investigated in rice plants. NO3‐‐promoted SR elongation, possibly due to short‐term signal perception and long‐term nutrient function. Compared with NH4+ condition, higher SL signalling/levels and less D53 protein were recorded in roots of NO3‐‐treated rice plants. In contrast to wild‐type (WT) plants, SR lengths of d mutants were less responsive to NO3‐ condition, and application of rac‐GR24 (SL analogue) restored SR length in d10 (SL‐biosynthesis mutant) but not in d3,d14 and d53 (SL‐responsive mutants), suggesting that higher SL signalling/levels participated in NO3‐‐induced root elongation. D53 interacted with SPL17, and inhibited SPL17‐mediated transactivation from PIN1b promoter. Mutation of SPL14/17 and PIN1b caused insensitivity of root elongation response to NO3‐ and rac‐GR24 applications. Therefore, we presented that perception of SLs by D14 led to degradation of D53 via the proteasome system, which released the suppression of SPL14/17‐modulated the transcription of PIN1b, and resulted in root elongation under NO3‐ supply."
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