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Authors: Haihai Wang, Yongcai Huang, Yujie Li, Yahui Cui, Xiaoli Xiang, Yidong Zhu, Qiong Wang, Xiaoqing Wang, Guangjin Ma, Qiao Xiao, Xing Huang, Xiaoyan Gao, Jiechen Wang, Xiaoduo Lu, Brian A. Larkins, Wenqin Wang and Yongrui Wu.
Nature Communications (2024
Editor's view: The mutation of ARFTF17 results in the development of flint kernel architecture in dent maize by reducing excessive pericarp length. This discovery holds significant potential for enhancing grain quality in elite, high-yielding dent maize hybrids.
Abstract: "Dent and flint kernel architectures are important characteristics that affect the physical properties of maize kernels and their grain end uses. The genes controlling these traits are unknown, so it is difficult to combine the advantageous kernel traits of both. We found mutation of ARFTF17 in a dent genetic background reduces IAA content in the seed pericarp, creating a flint-like kernel phenotype. ARFTF17 is highly expressed in the pericarp and encodes a protein that interacts with and inhibits MYB40, a transcription factor with the dual functions of repressing PIN1 expression and transactivating genes for flavonoid biosynthesis. Enhanced flavonoid biosynthesis could reduce the metabolic flux responsible for auxin biosynthesis. The decreased IAA content of the dent pericarp appears to reduce cell division and expansion, creating a shorter, denser kernel. Introgression of the ARFTF17 mutation into dent inbreds and hybrids improved their kernel texture, integrity, and desiccation, without affecting yield."
Authors: Junping He, Lu Yao, Lorenzo Pecoraro, Changxiao Liu, Juan Wang, Luqi Huang and Wenyuan Gao.
Critical Reviews in Biotechnology (2023)
Abstract: "Plants make different defense mechanisms in response to different environmental stresses. One common way is to produce secondary metabolites. Temperature is the main environmental factor that regulates plant secondary metabolites, especially flavonoids and terpenoids. Stress caused by temperature decreasing to 4–10 °C is conducive to the accumulation of flavonoids and terpenoids. However, the accumulation mechanism under cold stress still lacks a systematic explanation. In this review, we summarize three aspects of cold stress promoting the accumulation of flavonoids and terpenoids in plants, that is, by affecting (1) the content of endogenous plant hormones, especially jasmonic acid and abscisic acid; (2) the expression level and activity of important transcription factors, such as bHLH and MYB families. This aspect also includes post-translational modification of transcription factors caused by cold stress; (3) key enzyme genes expression and activity in the biosynthesis pathway, in addition, the rate-limiting enzyme and glycosyltransferases genes are responsive to cold stress. The systematic understanding of cold stress regulates flavonoids, and terpenoids will contribute to the future research of genetic engineering breeding, metabolism regulation, glycosyltransferases mining, and plant synthetic biology."
Authors: Jieting Wu, Sidi Lv, Lei Zhao, Tian Gao, Chang Yu, Jianing Hu and Fang Ma.
Planta (2023)
Main conclusion: This review summarizes the anti-stress effects of flavonoids in plants and highlights its role in the regulation of polar auxin transport and free radical scavenging mechanism.
Abstract: "As secondary metabolites widely present in plants, flavonoids play a vital function in plant growth, but also in resistance to stresses. This review introduces the classification, structure and synthetic pathways of flavonoids. The effects of flavonoids in plant stress resistance were enumerated, and the mechanism of flavonoids in plant stress resistance was discussed in detail. It is clarified that plants under stress accumulate flavonoids by regulating the expression of flavonoid synthase genes. It was also determined that the synthesized flavonoids are transported in plants through three pathways: membrane transport proteins, vesicles, and bound to glutathione S-transferase (GST). At the same time, the paper explores that flavonoids regulate polar auxin transport (PAT) by acting on the auxin export carrier PIN-FORMED (PIN) in the form of ATP-binding cassette subfamily B/P-glycoprotein (ABCB/PGP) transporter, which can help plants to respond in a more dominant form to stress. We have demonstrated that the number and location of hydroxyl groups in the structure of flavonoids can determine their free radical scavenging ability and also elucidated the mechanism by which flavonoids exert free radical removal in cells. We also identified flavonoids as signaling molecules to promote rhizobial nodulation and colonization of arbuscular mycorrhizal fungi (AMF) to enhance plant–microbial symbiosis in defense to stresses. Given all this knowledge, we can foresee that the in-depth study of flavonoids will be an essential way to reveal plant tolerance and enhance plant stress resistance."
Authors: Wenchao Zhao, Jingjing Liang, Huang Huang, Jinshan Yang, Jiaping Feng, Lulu Sun, Rui Yang, Mengjia Zhao, Jianli Wang and Shaohui Wang.
New Phytologist (2023)
Abstract: "JA is involved in the modulation of defence and growth activities in plants. The best-characterized growth-defence trade-offs stem from antagonistic crosstalk among hormones. In this study, we first confirmed that JA negatively regulates root-knot nematode (RKN) susceptibility via the root exudates (REs) of tomato plants. Omics and toxicological analyses implied that kaempferol, a type of flavonol, from REs has a negative effect on RKN infection. We demonstrated that SlMYB57 negatively regulated kaempferol contents in tomato roots, whereas SlMYB108/112 had the opposite effect. We revealed that JA fine-tuned the homeostasis of kaempferol via SlMYB-mediated transcriptional regulation and the interaction between SlJAZs and SlMYBs, thus ensuring a balance between lateral root (LR) development and RKN susceptibility. Overall, this work provides novel insights into JA-modulated LR development and RKN susceptibility mechanisms and elucidates a trade-off model mediated by JA in plants encountering stress."
Authors: Qi Chen, Xiaojun Pu, Xiaomin Li, Rongrong Li, Qian Yang, Xinjia Wang, Miao Guan and Zed Rengel.
Journal of Experimental Botany (2022)
Abstract: "Phytomelatonin is a new plant hormone, and its primary functions in plant growth and development remain relatively poorly appraised. Phytomelatonin is a master regulator of the reactive oxygen species (ROS) signaling and acts as a darkness signal in circadian stomatal closure. Plants exhibit at least three interrelated patterns of interactions between phytomelatonin and ROS production. Exogenous melatonin could induce flavonoid biosynthesis, which might be required for maintenance of antioxidant capacity under stress, after harvest and in leaf senescence conditions. However, several genetic studies provided direct evidence that phytomelatonin plays a negative role in the biosynthesis of flavonoids under normal growth conditions. Phytomelatonin delays flowering time in both dicot and monocot plants, probably via its receptor PMTR1 and interactions with the gibberellin (GA), strigolactone (SL) and ROS signaling pathways. Furthermore, phytomelatonin signaling also functions in hypocotyl and shoot growth in skotomorphogenesis and UV-B exposure; the G protein α-subunit (arabidopsis GPA1 and rice RGA1) and Constitutive Photomorphogenic1 (COP1) are important signal components during this process. Taken together, phytomelatonin acts as a darkness signal with important regulatory roles in circadian stomatal closure, flavonoid biosynthesis, flowering, and hypocotyl and shoot growth."
Authors: Bethany L. Richmond, Chloe L. Coelho, Helen Wilkinson, Joseph McKenna, Pélagie Ratchinski, Maximillian Schwarze, Matthew Frost, Beatriz Lagunas and Miriam L. Gifford.
Physiologia Plantarum (2022)
Abstract: "Strigolactones are the most recently discovered phytohormones, and their roles in root architecture and metabolism are not fully understood. Here, we investigated four MORE AXILLARY GROWTH (MAX) strigolactone mutants in Arabidopsis thaliana, max3-9, max4-1, max1-1 and max2-1, as well as the strigolactone receptor mutant d14-1 and karrikin receptor mutant kai2-2. By characterising max2-1 and max4-1, we found that variation in strigolactone biosynthesis modified multiple metabolic pathways in root tissue, including that of xyloglucan, triterpenoids, fatty acids and flavonoids. The transcription of key flavonoid biosynthetic genes, including TRANSPARENT TESTA4 (TT4) and TRANSPARENT TESTA5 (TT5) was downregulated in max2 roots and seedlings, indicating that the proposed MAX2 regulation of flavonoid biosynthesis has a widespread effect. We found an enrichment of BRI1-EMS-SUPPRESSOR 1 (BES1) targets among genes specifically altered in the max2 mutant, reflecting that the regulation of flavonoid biosynthesis likely occurs through the MAX2 degradation of BES1, a key brassinosteroid-related transcription factor. Finally, flavonoid accumulation decreased in max2-1 roots, supporting a role for MAX2 in regulating both strigolactone and flavonoid biosynthesis."
Authors: Chuanyong Xiong, Xiaoqing Li, Xin Wang, Jingxin Wang, Hans Lambers, Carroll P Vance, Jianbo Shen and Lingyun Cheng.
Annals of Botany (2022)
Abstract: "Background and Aims - Initiation of cluster roots in white lupin (Lupinus albus L.) under phosphorus (P) deficiency requires auxin signaling, whereas flavonoids inhibit auxin transport. However, little information is available about the interactions between P deficiency and flavonoids in terms of cluster-root formation in white lupin. Methods - Hydroponic and aeroponic systems were used to investigate the role of flavonoids in cluster-root formation, with or without 75 µM P supply. Key Results - Phosphorus-deficiency-induced flavonoid accumulation in cluster roots depended on developmental stage, based on in situ determination of fluorescence of flavonoids and flavonoid concentration. LaCHS8, which codes for a chalcone synthase isoform, was highly expressed in cluster roots, and silencing LaCHS8 reduced flavonoid production and rootlet density. Exogenous flavonoids suppressed cluster-root formation. Tissue-specific distribution of flavonoids in roots was altered by P deficiency, suggesting that P deficiency induced flavonoid accumulation, thus fine-tuning the effect of flavonoids on cluster-root formation. Furthermore, naringenin inhibited expression of an auxin-responsive DR5:GUS marker, suggesting an interaction of flavonoids and auxin in regulating cluster-root formation. Conclusions - Phosphorus deficiency triggered cluster-root formation through the regulation of flavonoid distribution, which fine-tuned an auxin response in the early stages of cluster-root development. These findings provide valuable insights into the mechanisms of cluster-root formation under P deficiency."
Authors: Hao Sun, Huiting Cui, Jiaju Zhang, Junmei Kang, Zhen Wang, Mingna Li, Fengyan Yi, Qingchuan Yang and Ruicai Long.
International Journal of Molecular Sciences (2021)
Abstract: "Bioactive gibberellic acids (GAs) are diterpenoid plant hormones that are biosynthesized through complex pathways and control various aspects of growth and development. Although GA biosynthesis has been intensively studied, the downstream metabolic pathways regulated by GAs have remained largely unexplored. We investigated Tnt1 retrotransposon insertion mutant lines of Medicago truncatula with a dwarf phenotype by forward and reverse genetics screening and phylogenetic, molecular, biochemical, proteomic and metabolomic analyses. Three Tnt1 retrotransposon insertion mutant lines of the gibberellin 3-beta-dioxygenase 1 gene (GA3ox1) with a dwarf phenotype were identified, in which the synthesis of GAs (GA3 and GA4) was inhibited. Phenotypic analysis revealed that plant height, root and petiole length of ga3ox1 mutants were shorter than those of the wild type (Medicago truncatula écotype R108). Leaf size was also much smaller in ga3ox1 mutants than that in wild-type R108, which is probably due to cell-size diminution instead of a decrease in cell number. Proteomic and metabolomic analyses of ga3ox1/R108 leaves revealed that in the ga3ox1 mutant, flavonoid isoflavonoid biosynthesis was significantly up-regulated, while nitrogen metabolism was down-regulated. Additionally, we further demonstrated that flavonoid and isoflavonoid biosynthesis was induced by prohexadione calcium, an inhibitor of GA3ox enzyme, and inhibited by exogenous GA3. In contrast, nitrogen metabolism was promoted by exogenous GA3 but inhibited by prohexadione calcium. The results of this study further demonstrated that GAs play critical roles in positively regulating nitrogen metabolism and transport and negatively regulating flavonoid biosynthesis through GA-mediated signaling pathways in leaves."
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Authors: Zhongbang Song, Lu Zhao, Wenna Ma, Zhongping Peng, Junli Shi, Feng Pan, Yulong Gao, Xueyi Sui, Zed Rengel, Qi Chen and Bingwu Wang.
Journal of Experimental Botany (2023)
Abstract: "Stomatal movement could be regulated by ABA signaling through synthesis of reactive oxygen species (ROS) in guard cells. By contrast, ethylene triggers biosynthesis of antioxidant flavonol to suppress ROS accumulation and prevent ABA-induced stomatal closure, but the underlying mechanism remains largely unknown. We isolated and characterized tobacco R2R3-MYB NtMYB184, belonging to the flavonol-specific SG7 subgroup. The RNAi suppression (KD line) and knockout (myb184) of NtMYB184 caused a down-regulation of flavonol biosynthetic genes and decreased the concentration of flavonol in tobacco leaves. Yeast one-hybrid assay, transactivation assay, EMSA and ChIP-qPCR demonstrated that NtMYB184 specifically binds to the promoters of flavonol biosynthetic genes via the MYBPLANT motifs. In tobacco, NtMYB184 regulates flavonol biosynthesis in guard cells to modulate ROS homeostasis and stomatal aperture. ABA-induced ROS production was accompanied by the suppression of NtMYB184 and flavonol biosynthesis, which may accelerate ABA-induced stomatal closure. Furthermore, ethylene stimulated the NtMYB184 expression and flavonol biosynthesis to suppress ROS accumulation and curb ABA-induced stomatal closure. In myb184, however, neither the flavonol and ROS concentrations nor the stomatal aperture varied between the ABA and ABA+ethylene treatments, indicating that NtMYB184 was indispensable for the antagonism between ethylene and ABA via regulating flavonol and ROS concentrations in guard cells."
Authors: Xueying Zhang, Linying Li, Yuqing He, Zhuoliang Lang, Yao Zhao, Han Tao, Qingsheng Li and Gaojie Hong.
Plant, Cell & Environment (2023)
Abstract: "High temperatures (HTs) seriously affect the yield and quality of tea. Catechins, derived from the flavonoid pathway, are characteristic compounds that contribute to the flavour of tea leaves. In this study, we first showed that the flavonoid content of tea leaves was significantly reduced under HT conditions via metabolic profiles; and then demonstrated that two transcription factors, CsHSFA1b and CsHSFA2 were activated by HT and negatively regulate flavonoid biosynthesis during HT treatment. Jasmonate (JA), a defensive hormone, plays a key role in plant adaption to environmental stress. However, little has been reported on its involvement in HT response in tea. Herein, we demonstrated that CsHSFA1b and CsHSFA2 activate CsJAZ6 expression through directly binding to heat shock elements in its promoter, and thereby repress the JA pathway. Most secondary metabolites are regulated by JA, including catechin in tea. Our study reported that CsJAZ6 directly interacts with CsEGL3 and CsTTG1 and thereby reduces catechin accumulation. From this, we proposed a CsHSFA-CsJAZ6-mediated HT regulation model of catechin biosynthesis. We also determined that negative regulation of the JA pathway by CsHSFAs and its homologues is conserved in Arabidopsis. These findings broaden the applicability of the regulation of JAZ by HSF transcription factors and further suggest the JA pathway as a valuable candidate for HT-resistant breeding and cultivation."
Authors: Hana Daryanavard, Anthony E. Postiglione, Joëlle K. Mühlemann and Gloria K. Muday.
Current Opinion in Plant Biology (2023)
Abstract: "Flavonols are plant-specialized metabolites with important functions in plant growth and development. Isolation and characterization of mutants with reduced flavonol levels, especially the transparent testa mutants in Arabidopsis thaliana, have contributed to our understanding of the flavonol biosynthetic pathway. These mutants have also uncovered the roles of flavonols in controlling development in above- and below-ground tissues, notably in the regulation of root architecture, guard cell signaling, and pollen development. In this review, we present recent progress made towards a mechanistic understanding of flavonol function in plant growth and development. Specifically, we highlight findings that flavonols act as reactive oxygen species (ROS) scavengers and inhibitors of auxin transport in diverse tissues and cell types to modulate plant growth and development and responses to abiotic stresses."
Authors: Chhana Ullah, Yen-Ho Chen, María A. Ortega and Chung-Jui Tsai.
Current Opinion in Plant Biology (2023)
Abstract: "The phytohormone salicylic acid (SA) is known to regulate plant immunity against pathogens. Plants synthesize SA via the isochorismate synthase (ICS) pathway or the phenylalanine ammonia-lyase (PAL) pathway. The ICS pathway has been fully characterized using Arabidopsis thaliana, a model plant that exhibits pathogen-inducible SA accumulation. Many species including Populus (poplar) depend instead on the partially understood PAL pathway for constitutive as well as pathogen-stimulated SA synthesis. Diversity of SA-mediated defense is also evident in SA accumulation, redox regulation, and interplay with other hormones like jasmonic acid. This review highlights the contrast between Arabidopsis and poplar, discusses potential drivers of SA diversity in plant defenses, and offers future research directions."
Authors: Zhongqin Zhang, Le Gao, Meiyu Ke, Zhen Gao, Tianli Tu, Laimei Huang, Jiaomei Chen, Yuefeng Guan, Xi Huang and Xu Chen.
Journal of Integrative Plant Biology (2022)
Abstract: "Crop breeding during the Green Revolution resulted in high yields largely due to the creation of plants with semi-dwarf architectures that could tolerate high-density planting. Although semi-dwarf varieties have been developed in rice, wheat and maize, none was reported in soybean (Glycine max), and few genes controlling plant architecture have been characterized in soybean. Here, we demonstrate that the auxin efflux transporter PINFORMED1 (GmPIN1), which determines polar auxin transport, regulates the leaf petiole angle in soybean. CRISPR-Cas9-induced Gmpin1abc and Gmpin1bc multiple mutants displayed a compact architecture with a smaller petiole angle than wild-type plants. GmPIN1 transcripts and auxin were distributed asymmetrically in the petiole base, with high levels of GmPIN1a/c transcript and auxin in the lower cells, which resulted in asymmetric cell expansion. By contrast, the (iso)flavonoid content was greater in the upper petiole cells than in the lower cells. Our results suggest that (iso)flavonoids inhibit GmPIN1a/c expression to regulate the petiole angle. Overall, our study demonstrates that a signal cascade that integrates (iso)flavonoid biosynthesis, GmPIN1a/c expression, auxin accumulation, and cell expansion in an asymmetric manner creates a desirable petiole curvature in soybean. This study provides a genetic resource for improving soybean plant architecture."
Abstract: Luis Morales-Quintana and Patricio Ramos.
International Journal of Molecular Sciences (2021)
Abstract: "Plants reorient the growth of affected organs in response to the loss of gravity vector. In trees, this phenomenon has received special attention due to its importance for the forestry industry of conifer species. Sustainable management is a key factor in improving wood quality. It is of paramount importance to understand the molecular and genetic mechanisms underlying wood formation, together with the hormonal and environmental factors that affect wood formation and quality. Hormones are related to the modulation of vertical growth rectification. Many studies have resulted in a model that proposes differential growth in the stem due to unequal auxin and jasmonate allocation. Furthermore, many studies have suggested that in auxin distribution, flavonoids act as molecular controllers. It is well known that flavonoids affect auxin flux, and this is a new area of study to understand the intracellular concentrations and how these compounds can control the gravitropic response. In this review, we focused on different molecular aspects related to the hormonal role in flavonoid homeostasis and what has been done in conifer trees to identify molecular players that could take part during the gravitropic response and reduce low-quality wood formation."
Authors: Yun Chen, Jing-Bo Zhang, Ning Wei, Zhi-Hao Liu, Yang Li, Yong Zheng and Xue-Bao Li.
Plant Molecular Biology (2021)
Key message: GhDRP1 acts as a negatively regulator to participate in response to drought stress possibly by modulating ABA signaling pathway and flavonoid biosynthesis pathway which affects stomata movement and thus water loss, ROS scavenging enzymes, and proline accumulation in cotton.
Abstract: "Type-2C protein phosphatases (PP2C) may play important roles in plant stress signal transduction. Here, we show the evidence that a cotton PP2C protein GhDRP1 participates in plant response to drought stress. GhDRP1 gene encodes an active type-2C protein phosphatase (PP2C) and its expression is significantly induced in cotton by drought stress. Compared with wild type, the GhDRP1 overexpression (OE) transgenic cotton and Arabidopsis displayed reduced drought tolerance, whereas GhDRP1-silenced (RNAi) cotton showed enhanced drought tolerance. Under drought stress, malondialdehyde content was lower, whereas superoxide dismutase and peroxidase activities, proline content, stomata closure and relative water content were higher in GhDRP1 RNAi plants compared with those in wild type. In contrast, GhDRP1 OE plants showed the opposite phenotype under the same conditions. Expression levels of some stress-related and flavonoid biosynthesis-related genes were altered in GhDRP1 transgenic plants under drought stress. Additionally, GhDRP1 protein could interact with other proteins such as PYLs, SNF1-related protein kinase and GLK1-like protein. Collectively, these data suggest that GhDRP1 participates in plant response to drought stress possibly by modulating ABA signaling pathway and flavonoid biosynthesis pathway which affects stomata movement and thus water loss, ROS scavenging enzymes, and proline accumulation in cotton."
Authors: Wanlong Yang, Yuxin Fan, Biying Dong, Zhihua Song, Hongyan Cao, Tingting Du, Tengyue Liu, Meng Qi, Lili Niu, Dong Meng, Qing Yang and Yujie Fu.
Environmental and Experimental Botany (2021)
Highlights: • Abscisic acid (ABA) enhanced drought resistance of pigeon pea • The content of flavonoids increased after the application of ABA • Abscisic acid (ABA) regulates the up-regulation of flavonoid synthesis genes • MYB and bHLH TFs may play a central regulatory role in flavonoid biosynthesis
Abstract: "Abscisic acid (ABA) plays an important role in drought resistance of plants. Plants subjected to drought stress often produce a large number of secondary metabolites. More and more studies indicate that secondary metabolites are directly related to plant stress resistance. However, there are few reports about the influence of ABA regulating secondary metabolism on drought. In our study, we found that as a pioneer tree species in karst landforms, the drought resistance can also be improved by ABA. ABA can reduce the stomatal opening of pigeon pea under drought stress and reduce the influx of H+ from the root tip. At the same time, we found that in ABA-treated pigeon pea, flavonoid metabolites accumulate in large amounts, especially genistein, genistin and pterostilbene. Through transcriptome sequencing analysis, it was found that after ABA treatment, flavonoids biosynthesis pathways changed significantly; among them, the key enzyme genes CHS, HIDH and ROMT in the biosynthesis pathway of genistein, genistin and pterostilbene were significantly up-regulated. According to the co-expression analysis in the transcriptome data, we screened that multiple MYB and bHLH transcription factors may be involved in the regulation of flavonoid accumulation. And the biosynthetic genes contained binding sites of related transcription factors. Through RT-PCR, we further analyzed the expression of MYB, bHLH and related biosynthetic genes after ABA treatment at different times, and found that they were all regulated by ABA. By High Performance Liquid Chromatography (HPLC) analysis, we found the increase of genistein, genistin and pterostilbene content in pigeon pea treated with ABA under drought stress. Through hairy root transgenic analysis, We found that CcMYB114 regulate drought resistance by modulating the expression of CcHIDH1 and CcHIDH3, and then regulating genistein and genistin accumulation in pigeon pea. This study provides evidence to analyze the regulation of ABA in pigeon pea on the metabolism of flavonoids and thus affect its drought resistance."
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