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Authors: Mingfeng Zhang, Xiao Luo, Wei He, Min Zhang, Zhirong Peng, Huafeng Deng and Junjie Xing.
Plants (2024)
Abstract: "JAZ proteins function as transcriptional regulators that form a jasmonic acid–isoleucine (JA-Ile) receptor complex with coronatine insensitive 1 (COI1) and regulate plant growth and development. These proteins also act as key mediators in signal transduction pathways that activate the defense-related genes. Herein, the role of OsJAZ4 in rice blast resistance, a severe disease, was examined. The mutation of OsJAZ4 revealed its significance in Magnaporthe oryzae (M. oryzae) resistance and the seed setting rate in rice. In addition, weaker M. oryzae-induced ROS production and expression of the defense genes OsO4g10010, OsWRKY45, OsNAC4, and OsPR3 was observed in osjaz4 compared to Nipponbare (NPB); also, the jasmonic acid (JA) and gibberellin4 (GA4) content was significantly lower in osjaz4 than in NPB. Moreover, osjaz4 exhibited a phenotype featuring a reduced seed setting rate. These observations highlight the involvement of OsJAZ4 in the regulation of JA and GA4 content, playing a positive role in regulating the rice blast resistance and seed setting rate."
Authors: Karen Velandia, Alejandro Correa-Lozano, Peter M. McGuiness, James B. Reid and Eloise Foo.
bioRxiv (2023)
Abstract: "Gibberellins have a profound influence on the formation of lateral root organs. However, the precise role this hormone plays in the cell-specific events during lateral root formation, rhizobial infection and nodule organogenesis, including interactions with auxin and cytokinin, is not clear. In this study, we performed epidermal- and endodermal-specific complementation of the severely gibberellin-deficient na pea (Pisum sativum) mutant with Agrobacterium rhizogenes. Gibberellin mutants were used to examine the spatial expression pattern of cytokinin (TCSn) and auxin (DR5) responsive promoters and hormone levels. We found that gibberellins produced in the endodermis promotes lateral root and nodule organogenesis and can induce a mobile signal(s) that suppresses rhizobial infection. In contrast, epidermal-derived gibberellins suppress infection but have little influence on root or nodule development. Gibberellins suppress the cytokinin-responsive TCSn promoter in the cortex and are required for normal auxin activation during nodule primordia formation. Our findings indicate that GA regulates the checkpoints between infection thread penetration of the cortex and invasion of nodule primordial cells, and also promotes the subsequent progression of nodule development. It appears that GA may limit the progression and branching of infection threads in the cortex by restricting cytokinin response and may activate auxin response to promote nodule primordia development".
Authors: Gaochen Jin, Jinfeng Qi, Hongyue Zu, Shuting Liu, Jonathan Gershenzon, Yonggen Lou, Ian T Baldwin and Ran Li.
The Plant Cell (2023)
Abstract: "Plant defense against herbivores is costly and often associated with growth repression. The phytohormone jasmonate (JA) plays a central role in prioritizing defense over growth during herbivore attack, but the underlying mechanisms remain unclear. When brown planthoppers (BPH, Nilaparvata lugens) attack rice (Oryza sativa), growth is dramatically suppressed. BPH infestation also increases inactive gibberellin (GA) levels and transcripts of GA 2-oxidase (GA2ox) genes, two (GA2ox3 and GA2ox7) of which encode enzymes that catalyze the conversion of bioactive GAs to inactive GAs in vitro and in vivo. Mutation of these GA2oxs diminishes BPH-elicited growth restriction without affecting BPH resistance. Phytohormone profiling and transcriptome analyses revealed that GA2ox-mediated GA catabolism was enhanced by JA signaling. The transcript levels of GA2ox3 and GA2ox7 were significantly attenuated under BPH attack in JA biosynthesis (allene oxide cyclase, aoc) or signaling-deficient (myc2) mutants. In contrast, GA2ox3 and GA2ox7 expression was increased in MYC2 overexpression lines. MYC2 directly binds to the G-boxes in the promoters of both GA2ox genes to regulate their expression. We conclude that JA signaling simultaneously activates defense responses and GA catabolism to rapidly optimize resource allocation in attacked plants and provides a mechanism for phytohormone crosstalk."
Authors: Chihiro Miura, Yuki Furui, Tatsuki Yamamoto, Yuri Kanno, Masaya Honjo, Katsushi Yamaguchi, Kenji Suetsugu, Takahiro Yagame, Mitsunori Seo, Shuji Shigenobu, Masahide Yamato and Hironori Kaminaka.
bioRxiv (2023)
Abstract: "Orchids parasitically depend on external nutrients from mycorrhizal fungi for seed germination. Previous findings suggest that orchids utilize a genetic system of mutualistic arbuscular mycorrhizal (AM) symbiosis to establish parasitic symbiosis. In AM symbiosis, recent studies have revealed that the plant hormone gibberellin (GA) negatively affects fungal colonization and development. Although previous studies imply that GA is important for orchid mycorrhizal symbiosis, the molecular mechanism of seed germination in which mycorrhizal symbiosis co-occurs remains unclear because, in AM plants, GA regulates seed germination and symbiosis positively and negatively, respectively. To elucidate this conflict, we investigated the effect of GA on Bletilla striata seed germination and mycorrhizal symbiosis using asymbiotic and symbiotic germination methods. Additionally, we compared the transcriptome profiles between asymbiotically and symbiotically germinated seeds. Exogenous GA negatively affected seed germination and fungal colonization, and endogenous bioactive GA was actively converted to the inactive form during seed germination. Transcriptome analysis showed that B. striata shared many of the induced genes between asymbiotically and symbiotically germinated seeds, including GA metabolism- and signaling-related genes and AM-specific marker homologs. Our study suggests that orchids have evolved in a manner that they do not use bioactive GA as a positive regulator of seed germination and instead, auto-activate the mycorrhizal symbiosis pathway through GA inactivation to accept the fungal partner immediately during seed germination."
Authors: Hao-Nan Wang, Xia Ke, Jun-Ping Zhou, Zhi-Qiang Liu and Yu-Guo Zheng.
World Journal of Microbiology and Biotechnology (2022)
Abstract: "The plant growth hormone gibberellic acid (GA3), as one of the representative secondary metabolites, is widely used in agriculture, horticulture and brewing industry. GA3 is detected in both plants and several fungi with the ability to stimulate plant growth. Currently, the main mode of industrial production of GA3 is depended on the microbial fermentation via long-period submerged fermentation using Fusarium fujikuroi as the only producing strain, qualified for its natural productivity. However, the demand of large-sale industrialization of GA3 was still restricted by the low productivity. The biosynthetic route of GA3 in F. fujikuroi is now well-defined. Furthermore, the multi-level regulation mechanisms involved in the whole network of GA3 production have also been gradually unveiled by the past two decades based on the identification and characterization of several global regulators and their mutual functions. Combined with the quick development of genetic manipulation techniques, the rational modification of producing strain F. fujikuroi development become practical for higher productivity achievement. Herein, we review the latest advances in the molecular regulation of GA3 biosynthesis in F. fujikuroi and conclude a comprehensive network involving nitrogen depression, global regulator, histone modification and G protein signaling pathway. Correspondingly, the bioengineering strategies covering conventional random mutation, genetic manipulating platform development, metabolic edition and fermentation optimization were also systematically proposed."
Authors: Wenxiu Ma, Zhiqian Pang, Xiaoen Huang, Jin Xu, Sheo Shankar Pandey, Jinyun Li, Diann S. Achor, Fernanda N. C. Vasconcelos, Connor Hendrich, Yixiao Huang, Wenting Wang, Donghwan Lee, Daniel Stanton and Nian Wang.
Nature Communications (2022)
Editor's view: "Huanglongbing is a devastating disease of citrus, caused by phloem-colonizing bacteria. Here, the authors present evidence that the disease is the result of an exacerbated immune response to the infection, including production of reactive oxygen species, and that antioxidants and a growth-promoting hormone can mitigate disease symptoms."
Abstract: "Huanglongbing (HLB) is a devastating disease of citrus, caused by the phloem-colonizing bacterium Candidatus Liberibacter asiaticus (CLas). Here, we present evidence that HLB is an immune-mediated disease. We show that CLas infection of Citrus sinensis stimulates systemic and chronic immune responses in phloem tissue, including callose deposition, production of reactive oxygen species (ROS) such as H2O2, and induction of immunity-related genes. The infection also upregulates genes encoding ROS-producing NADPH oxidases, and downregulates antioxidant enzyme genes, supporting that CLas causes oxidative stress. CLas-triggered ROS production localizes in phloem-enriched bark tissue and is followed by systemic cell death of companion and sieve element cells. Inhibition of ROS levels in CLas-positive stems by NADPH oxidase inhibitor diphenyleneiodonium (DPI) indicates that NADPH oxidases contribute to CLas-triggered ROS production. To investigate potential treatments, we show that addition of the growth hormone gibberellin (known to have immunoregulatory activities) upregulates genes encoding H2O2-scavenging enzymes and downregulates NADPH oxidases. Furthermore, foliar spray of HLB-affected citrus with gibberellin or antioxidants (uric acid, rutin) reduces H2O2 concentrations and cell death in phloem tissues and reduces HLB symptoms. Thus, our results indicate that HLB is an immune-mediated disease that can be mitigated with antioxidants and gibberellin."
Authors: Chetan Keswani, Satyendra Pratap Singh, Carlos García-Estrada, Samia Mezaache-Aichour, Travis R. Glare, Rainer Borriss, Vishnu D. Rajput, Tatiana M. Minkina, Aurelio Ortiz and Estibaliz Sansinenea.
Journal of Applied Microbiology (2022)
Abstract: "Soil microbes promote plant growth through several mechanisms such as secretion of chemical compounds including plant growth hormones. Among the phytohormones, auxins, ethylene, cytokinins, abscisic acid and gibberellins are the best understood compounds. Gibberellins were first isolated in 1935 from the fungus Gibberella fujikuroi and are synthesized by several soil microbes. The effect of gibberellins on plant growth and development has been studied, as has the biosynthesis pathways, enzymes, genes and their regulation. This review revisits the history of gibberellin research highlighting microbial gibberellins and their effects on plant health with an emphasis on the early discoveries and current advances that can find vital applications in agricultural practices."
Authors: Akira Akamatsu, Miwa Nagae, Yuka Nishimura, Daniela Romero Montero, Satsuki Ninomiya, Mikiko Kojima, Yumiko Takebayashi, Hitoshi Sakakibara, Masayoshi Kawaguchi and Naoya Takeda.
The Plant Journal (2020)
Abstract: "Legumes and nitrogen‐fixing rhizobial bacteria establish root nodule symbiosis, which is orchestrated by several plant hormones. Exogenous addition of biologically active gibberellic acid (GA) is known to inhibit root nodule symbiosis. However, the precise role of GA has not been elucidated because of the trace amounts of these hormones in plants and the multiple functions of GAs. Here, we found that GA signaling acts as a key regulator in a long‐distance negative‐feedback system of root nodule symbiosis called autoregulation of nodulation (AON). GA biosynthesis is activated during nodule formation in and around the nodule vascular bundles, and bioactive GAs accumulate in the nodule. In addition, GA signaling induces expression of the symbiotic transcription factor NODULE INCEPTION (NIN) via a cis‐acting region on the NIN promoter. Mutants with deletions of this cis‐acting region have increased susceptibility to rhizobial infection and reduced GA‐induced CLE‐RS1 and CLE‐RS2 expression, suggesting that the inhibitory effect of GAs occurs through AON. This is supported by the GA‐insensitive phenotypes of an AON‐defective mutant of HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1), and a reciprocal grafting experiment. Thus, endogenous GAs induce NIN expression via its GA‐responsive cis‐acting region, then the GA‐induced NIN activates the AON system to regulate nodule formation."
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Authors: Chihiro Miura, Yuki Furui, Tatsuki Yamamoto, Yuri Kanno, Masaya Honjo, Katsushi Yamaguchi, Kenji Suetsugu, Takahiro Yagame, Mitsunori Seo, Shuji Shigenobu, Masahide Yamato and Hironori Kaminaka.
Plant Physiology (2023)
Abstract: "Orchids parasitically depend on external nutrients from mycorrhizal fungi for seed germination. Previous findings suggest that orchids utilize a genetic system of mutualistic arbuscular mycorrhizal (AM) symbiosis, in which the plant hormone gibberellin (GA) negatively affects fungal colonization and development, to establish parasitic symbiosis. Although GA generally promotes seed germination in photosynthetic plants, previous studies have reported low sensitivity of GA in seed germination of mycoheterotrophic orchids where mycorrhizal symbiosis occurs concurrently. To elucidate the connecting mechanisms of orchid seed germination and mycorrhizal symbiosis at the molecular level, we investigated the effect of GA on a hyacinth orchid (Bletilla striata) seed germination and mycorrhizal symbiosis using asymbiotic and symbiotic germination methods. Additionally, we compared the transcriptome profiles between asymbiotically and symbiotically germinated seeds. Exogenous GA negatively affected seed germination and fungal colonization, and endogenous bioactive GA was actively converted to the inactive form during seed germination. Transcriptome analysis showed that B. striata shared many of the induced genes between asymbiotically and symbiotically germinated seeds, including GA metabolism- and signaling-related genes and AM-specific marker homologs. Our study suggests that orchids have evolved in a manner that they do not use bioactive GA as a positive regulator of seed germination and instead auto-activate the mycorrhizal symbiosis pathway through GA inactivation to accept the fungal partner immediately during seed germination."
Author: Lucas Frungillo.
The Plant Cell (2023)
Excerpts: "The brown planthopper (BPH), Nilaparvata lugens, is a major threat to rice (Oryza sativa)."
"Because the phytohormone gibberellic acid (GA) regulates plant growth and development, the authors sought to investigate the impact of BPH feeding on GA levels in rice. Hormonal profiling by liquid chromatography–mass spectrometry (LC-MS) revealed lower levels of GA bioactive forms in BPH-attacked rice compared to control plants. Accordingly, overexpression of the GA catabolic genes GA2ox3 and GA2ox7 resulted in lower levels of bioactive GA and reduced growth as compared to wild-type plants (see Figure), suggesting that herbivore attack triggers the catabolism of bioactive GAs in rice."
"Collectively, Jin et al. (2023) provide compelling evidence that the MYC2-GA2ox module orchestrates JA-GA hormonal crosstalk in rice during defense responses against BPH attack. The mechanistic insights presented in this study open exciting new directions for the investigation of hormonal crosstalk in plants and provide a framework for improving resistance to pests without yield penalties in rice.
Authors: Jia Xin Yap and Yuichiro Tsuchiya.
Plant and Cell Physiology (2023)
Abstract: "Dormant seeds of a root parasitic plant Striga hermonthica sense strigolactones from host plants as environmental cues for germination. This process is mediated by diversified member of strigolactone receptors encoded by HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE2 genes. It is known that warm and moist treatment of seed conditioning gradually turns dormant Striga seeds competent to respond strigolactones, while the mechanism behind it has been poorly understood. In this report, we show that plant hormone gibberellins increase the strigolactone-competence by up-regulating mRNA expressions of the major strigolactone receptors during the conditioning period. This idea was supported by poor germination phenotype when gibberellin biosynthesis is depleted by paclobutrazol during conditioning. Moreover, live-imaging with fluorogenic strigolactone-mimic, yoshimulactone green W, revealed that paclobutrazol treatment during conditioning caused aberrant dynamics of strigolactone perception after germination. These observations revealed an indirect role of gibberellins to the seed germination in Striga, which is contrastive to their roles as dominant germination stimulating hormone in non-parasitic plants. We propose a model of how the role of gibberellins become indirect during the evolution of parasitism in plants. Our work also highlight the potential role for gibberellins in field application, for instance, elevating the sensitivity of the seeds towards strigolactones in the current suicidal germination approach to alleviate the agricultural threats caused by this parasite in Africa."
Authors: Lulu Li, Hehong Zhang, Zihang Yang, Chen Wang, Shanshan Li, Chen Cao, Tongsong Yao, Zhongyan Wei, Yanjun Li, Jianping Chen and Zongtao Sun.
Nature Communications (2022)
Editor's view: Plant viruses adopt diverse strategies to inhibit host antiviral defense. Here the authors show that multiple different effectors from various rice viruses interfere with host gibberellin signaling by targeting the DELLA protein SLR1.
Abstract: "Plant viruses adopt diverse virulence strategies to inhibit host antiviral defense. However, general antiviral defense directly targeted by different types of plant viruses have rarely been studied. Here, we show that the single rice DELLA protein, SLENDER RICE 1 (SLR1), a master negative regulator in Gibberellin (GA) signaling pathway, is targeted by several different viral effectors for facilitating viral infection. Viral proteins encoded by different types of rice viruses all directly trigger the rapid degradation of SLR1 by promoting association with the GA receptor OsGID1. SLR1-mediated broad-spectrum resistance was subverted by these independently evolved viral proteins, which all interrupted the functional crosstalk between SLR1 and jasmonic acid (JA) signaling. This decline of JA antiviral further created the advantage of viral infection. Our study reveals a common viral counter-defense strategy in which different types of viruses convergently target SLR1-mediated broad-spectrum resistance to benefit viral infection in the monocotyledonous crop rice.
Authors: Ryan S. Nett, Kelly S. Bender and Reuben J. Peters.
The ISME Journal (2022)
Abstract: "Plant-associated microbes have evolved the ability to independently produce gibberellin (GA) phytohormones as a mechanism to influence their host. Indeed, GA was first discovered as a metabolite from the fungal rice pathogen Gibberella fujikuroi, which uses it as a virulence factor. Though some bacterial plant pathogens similarly use GA to promote infection, symbiotic nitrogen-fixing bacteria (rhizobia), which inhabit the root nodules of legumes, also can produce GA, suggesting a role in symbiosis. The bacterial GA biosynthetic operon has been identified, but in rhizobia this typically no longer encodes the final metabolic gene (cyp115), so that these symbionts can only produce the penultimate intermediate GA9. Here, we demonstrate that soybean (Glycine max) expresses functional GA 3-oxidases (GA3ox) within its nodules, which have the capability to convert GA9 produced by the enclosed rhizobial symbiont Bradyrhizobium diazoefficiens to bioactive GA4. This rhizobia-derived GA is demonstrated to cause an increase in nodule size and decrease in the number of nodules. The increase in individual nodule size correlates to greater numbers of bacterial progeny within a nodule, thereby providing a selective advantage to rhizobia that produce GA during the rhizobia-legume symbiosis. The expression of GA3ox in nodules and resultant nodulation effects of the GA product suggests that soybean has co-opted control of bioactive GA production, and thus nodule size, for its own benefit. Thus, our results suggest rhizobial GA biosynthesis has coevolved with host plant metabolism for cooperative production of a phytohormone that influences nodulation in a mutually beneficial manner."
Authors: Anish Kundu, Shruti Mishra, Pritha Kundu, Abhimanyu Jogawat and Jyothilakshmi Vadassery.
Plant Physiology (2021)
Abstract: "Growth promotion induced by the endosymbiont Piriformospora indica has been observed in various plants; however, except growth phytohormones, specific functional metabolites involved in P. indica-mediated growth promotion are unknown. Here, we used a GC-MS based untargeted metabolite analysis to identify tomato (Solanum lycopersicum) metabolites whose levels were altered during P. indica-mediated growth promotion. Metabolomic multivariate analysis revealed several primary metabolites with altered levels, with putrescine induced most significantly in roots during the interaction. Further, our results indicated that P. indica modulates the arginine decarboxylase (ADC)-mediated putrescine biosynthesis pathway via induction of SlADC1 in tomato. P. indica did not promote growth in Sladc1-VIGS (virus-induced gene silencing of SlADC1) lines of tomato tomato and showed less colonization. Furthermore, using LC-MS/MS we showed that putrescine promoted growth by elevation of auxin (indole-3-acetic acid) and gibberellin (GA4, GA7) levels in tomato. In Arabidopsis (Arabidopsis thaliana) adc knock-out mutants, P. indica colonization also decreased and showed no plant growth promotion, and this response was rescued upon exogenous application of putrescine. Putrescine is also important for hyphal growth of P. indica, indicating that it is co-adapted by both host and microbe. Taken together, we conclude that putrescine is an essential metabolite and its biosynthesis in plants is crucial for P. indica-mediated plant growth promotion and fungal growth."
Authors: Raphaella Hull, Jeongmin Choi and Uta Paszkowski.
Current Opinion in Plant Biology (2021)
Abstract: "The evolutionarily ancient α/β hydrolase DWARF14-LIKE (D14L) is indispensable for the perception of beneficial arbuscular mycorrhizal (AM) fungi in the rhizosphere, and for a range of developmental processes. Variants of D14L recognise natural strigolactones and the smoke constituent karrikin, both classified as butenolides, and additional unknown ligand(s), critical for symbiosis and development. Recent advances in the understanding of downstream effects of D14L signalling include biochemical evidence for the degradation of the repressor SMAX1. Indeed, genetic removal of rice SMAX1 leads to the de-repression of symbiosis programmes and to the simultaneous increase in strigolactone production. As strigolactones are key to attraction of the fungus in the rhizosphere, the D14L signalling pathway appears to coordinate fungal stimulation and root symbiotic competency. Here, we discuss the possible integrative roles of D14L signalling in conditioning plants for AM symbiosis."
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