Pub Date : 2024-07-27DOI: 10.1007/s00344-024-11385-w
Qiaoli Ma, Xinghua Liang
Licorice roots can release low-molecular-weight oxalic acid (OA). However, the allelopathic effects of OA on licorice are unknown. This study presents an investigation of the effects of exogenous OA treatment on licorice roots through transcriptomic and physiological analyses. Transcriptomic analysis demonstrated that following OA treatment, differentially expressed genes (DEGs) were primarily involved in the phenylpropanoid metabolism pathway. At 6 h, the expression levels of genes associated with this pathway, such as PAL, CHS, POD, cellulase, CPY, MYB, and bHLH, were upregulated. The metabolism of related metabolites, such as flavonoids and lignin, also increased. These findings suggest that the phenylpropanoid metabolism pathway may play a significant role in the response to OA treatment. In addition, the activities of GST, CAT, and POD markedly increased, whereas the content of H2O2 gradually decreased, indicating that OA can activate the antioxidant protective capabilities of licorice roots. These findings suggest that OA may enhance the antioxidant defense of licorice root, as well as the effectiveness of its flavonoid constituents (to a certain degree). Our findings provide valuable theoretical insight into the allelopathic effects of licorice roots.
甘草根能释放低分子量草酸(OA)。然而,OA 对甘草的等位病理效应尚不清楚。本研究通过转录组学和生理学分析,研究了外源 OA 处理对甘草根的影响。转录组分析表明,OA 处理后,差异表达基因(DEGs)主要涉及苯丙类代谢途径。在 6 小时内,与该途径相关的基因,如 PAL、CHS、POD、纤维素酶、CPY、MYB 和 bHLH 的表达水平上调。黄酮类化合物和木质素等相关代谢物的代谢也有所增加。这些研究结果表明,苯丙类代谢途径可能在OA治疗反应中发挥了重要作用。此外,GST、CAT 和 POD 的活性明显提高,而 H2O2 的含量则逐渐降低,这表明 OA 可以激活甘草根的抗氧化保护能力。这些研究结果表明,OA 可增强甘草根的抗氧化防御能力,并在一定程度上增强其黄酮类成分的功效。我们的研究结果为了解甘草根的等位效应提供了宝贵的理论依据。
{"title":"Transcriptome Analysis Revealed that Oxalic Acid in Exogenous Licorice Root Exudates Can Stimulate the Phenylpropane Metabolic Pathway","authors":"Qiaoli Ma, Xinghua Liang","doi":"10.1007/s00344-024-11385-w","DOIUrl":"https://doi.org/10.1007/s00344-024-11385-w","url":null,"abstract":"<p>Licorice roots can release low-molecular-weight oxalic acid (OA). However, the allelopathic effects of OA on licorice are unknown. This study presents an investigation of the effects of exogenous OA treatment on licorice roots through transcriptomic and physiological analyses. Transcriptomic analysis demonstrated that following OA treatment, differentially expressed genes (DEGs) were primarily involved in the phenylpropanoid metabolism pathway. At 6 h, the expression levels of genes associated with this pathway, such as <i>PAL</i>, <i>CHS</i>, <i>POD</i>, <i>cellulase</i>, <i>CPY</i>, <i>MYB</i>, and <i>bHLH</i>, were upregulated. The metabolism of related metabolites, such as flavonoids and lignin, also increased. These findings suggest that the phenylpropanoid metabolism pathway may play a significant role in the response to OA treatment. In addition, the activities of GST, CAT, and POD markedly increased, whereas the content of H<sub>2</sub>O<sub>2</sub> gradually decreased, indicating that OA can activate the antioxidant protective capabilities of licorice roots. These findings suggest that OA may enhance the antioxidant defense of licorice root, as well as the effectiveness of its flavonoid constituents (to a certain degree). Our findings provide valuable theoretical insight into the allelopathic effects of licorice roots.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"162 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769317","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Potassium sulfate (K2SO4) or 2,4-Epibrassinolide (EBL) mediated response to cadmium (Cd) stress in plants has been widely reported, but the joint effect both on plants in response to Cd stress remains obscure. Herein, our results showed the combined application of K2SO4 (10 mM) and EBL (0.2 μM) on tobacco plants under Cd stress (CdCl2, 100 μM) relieved Cd toxicity by improving the activities of AOEs and reducing the contents of decreasing superoxide (H2O2 and O2−) and cadmium ion. As a result, the synergetic application of K2SO4 and EBL protected the integrity of chloroplast, which ensured a normal process of photosynthesis without a significant decrease in photosynthetic pigment content. Additionally, the combined application of K2SO4 and EBL also inhibited the expression of the Cd transport-related gene NtNramp1 and enhanced the Cd efflux-related gene NtHMA2. Moreover, the combined treatment of EBL associated with K2SO4 also effectively reduced the Cd accumulation in tobacco leaves under Cd stress compared with the groups treated separately, which implied a potentially synergistic role of EBL and K2SO4 in alleviating Cd toxicity in tobacco plants. This study provides a theoretical reference for the further analysis of the molecular mechanism of K2SO4 and EBL in jointly mediating the response to heavy metals in plants.
{"title":"Combined Application of 2,4-Epibrassinolide and K2SO4 Improved the Cadmium Tolerance in Tobaccos by Protecting Chloroplast and Reducing Cd Accumulation","authors":"Yalin Yang, Lijun Qin, Piao Wu, Xiangnan Qin, Yaxuan Xiang, Xian Gong","doi":"10.1007/s00344-024-11427-3","DOIUrl":"https://doi.org/10.1007/s00344-024-11427-3","url":null,"abstract":"<p>Potassium sulfate (K<sub>2</sub>SO<sub>4</sub>) or 2,4-Epibrassinolide (EBL) mediated response to cadmium (Cd) stress in plants has been widely reported, but the joint effect both on plants in response to Cd stress remains obscure. Herein, our results showed the combined application of K<sub>2</sub>SO<sub>4</sub> (10 mM) and EBL (0.2 μM) on tobacco plants under Cd stress (CdCl<sub>2</sub>, 100 μM) relieved Cd toxicity by improving the activities of AOEs and reducing the contents of decreasing superoxide (H<sub>2</sub>O<sub>2</sub> and O<sub>2</sub><sup>−</sup>) and cadmium ion. As a result, the synergetic application of K<sub>2</sub>SO<sub>4</sub> and EBL protected the integrity of chloroplast, which ensured a normal process of photosynthesis without a significant decrease in photosynthetic pigment content. Additionally, the combined application of K<sub>2</sub>SO<sub>4</sub> and EBL also inhibited the expression of the Cd transport-related gene <i>NtNramp1</i> and enhanced the Cd efflux-related gene <i>NtHMA2</i>. Moreover, the combined treatment of EBL associated with K<sub>2</sub>SO<sub>4</sub> also effectively reduced the Cd accumulation in tobacco leaves under Cd stress compared with the groups treated separately, which implied a potentially synergistic role of EBL and K<sub>2</sub>SO<sub>4</sub> in alleviating Cd toxicity in tobacco plants. This study provides a theoretical reference for the further analysis of the molecular mechanism of K<sub>2</sub>SO<sub>4</sub> and EBL in jointly mediating the response to heavy metals in plants.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"34 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769320","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-24DOI: 10.1007/s00344-024-11426-4
Qi Sun, Bei Zhang, Lin Xiang, Yanping Wang, Zhulong Chan
Tulips are mainly asexually propagated by bulbs that are modified underground stems. Hormones, including auxin, play pivotal roles during plant development. In this study, we investigated the roles of the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TgTIR1) in tulip bulb growth. TgTIR1 promoter activity analysis showed that it is most abundant in fast growing tissues including hypocotyl, cotyledons, and lateral root in Arabidopsis. Expression of TgTIR1 in Arabidopsis activated lateral organ boundary domain (LBD) transcription factors to promote the outgrowth of axillary branches and lateral roots. TgTIR1 transgenic plants also exhibited increased primary root length, plant height and leaf width. Moreover, downregulation of endogenous TgTIR1 through virus-induced gene silencing (VIGS) inhibited the growth of tulip plants and daughter bulbs. Exogenous auxin promoted while the auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA) repressed tulip daughter bulb growth. This study offered evidence that the auxin pathway was involved in lateral root initiation and tulip bulb growth.
{"title":"Auxin Receptor TRANSPORT INHIBITOR RESPONSE1 Promotes Tulip Plant Growth and Bulb Swelling","authors":"Qi Sun, Bei Zhang, Lin Xiang, Yanping Wang, Zhulong Chan","doi":"10.1007/s00344-024-11426-4","DOIUrl":"https://doi.org/10.1007/s00344-024-11426-4","url":null,"abstract":"<p>Tulips are mainly asexually propagated by bulbs that are modified underground stems. Hormones, including auxin, play pivotal roles during plant development. In this study, we investigated the roles of the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TgTIR1) in tulip bulb growth. <i>TgTIR1</i> promoter activity analysis showed that it is most abundant in fast growing tissues including hypocotyl, cotyledons, and lateral root in Arabidopsis. Expression of <i>TgTIR1</i> in Arabidopsis activated lateral organ boundary domain (LBD) transcription factors to promote the outgrowth of axillary branches and lateral roots. <i>TgTIR1</i> transgenic plants also exhibited increased primary root length, plant height and leaf width. Moreover, downregulation of endogenous <i>TgTIR1</i> through virus-induced gene silencing (VIGS) inhibited the growth of tulip plants and daughter bulbs. Exogenous auxin promoted while the auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA) repressed tulip daughter bulb growth. This study offered evidence that the auxin pathway was involved in lateral root initiation and tulip bulb growth.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"111 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769335","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The beneficial effects of endophytes on plant growth, development and yield are well known. Modulating plant growth-promoting substances and ameliorating biotic and abiotic stresses are some of the key mechanisms that are deployed by endophytes to facilitate host growth and defence. However, the understanding of the plant’s genome response to their presence is still limited. Therefore, this study provides an insight into the microbiome of B. juncea seeds as well as leaves, and its impact on plant growth and development. It also correlates their presence with the changes in plant. Removal of seed-borne culturable endophytes resulted in trade-off of accelerated growth with decreased biomass. 16S metagenomics revealed that bacterial endophyte diversity and density varied with stage of the plant. We found that 22 endophytic genera including Enterococcus, Halobacteroides, Planktothrix and Streptomyces were observed irrespective of Bavistin treatment and age of the plant. Removal of culturable endophytes also led to downregulation of crucial genes involved in growth, photosynthesis (Photosystem I assembly protein, Photosystem II reaction center protein and Rubisco), transport (nitrate transporter; NRT) and regulation of plant hormones (auxin homeostasis and signalling; CYP83A1) in B. juncea. To the best of our knowledge, this is the first report of the response of plant’ transcriptome to changes in endophyte composition indicating a strong possibility of host gene regulation by the endophytic partner. The exact mechanism of the same needs to be further explored.
内生菌对植物生长、发育和产量的有益影响众所周知。调节植物生长促进物质、改善生物和非生物胁迫是内生菌促进宿主生长和防御的一些关键机制。然而,人们对植物基因组对内生菌存在的反应的了解仍然有限。因此,本研究深入探讨了君子兰种子和叶片的微生物组及其对植物生长和发育的影响。研究还将它们的存在与植物的变化联系起来。去除种子中可培养的内生菌会导致加速生长与生物量下降的权衡。16S 元基因组学显示,细菌内生菌的多样性和密度随植物的生长阶段而变化。我们发现,无论巴维司汀的处理方法和植物的年龄如何,都能观察到 22 个内生菌属,包括肠球菌属(Enterococcus)、哈洛巴氏杆菌属(Halobacteroides)、扁虱属(Planktothrix)和链霉菌属(Streptomyces)。清除可培养的内生菌还会导致君子兰中参与生长、光合作用(光系统 I 组装蛋白、光系统 II 反应中心蛋白和 Rubisco)、运输(硝酸盐转运体;NRT)和植物激素调控(辅助素平衡和信号传导;CYP83A1)的关键基因下调。据我们所知,这是首次报道植物转录组对内生菌成分变化的反应,表明宿主基因很有可能受到内生菌伙伴的调控。其确切机制还有待进一步探讨。
{"title":"Molecular Evidence of Crosstalk Between Bacterial Endophytes and Plant Transcriptome in Brassica juncea","authors":"Garima Sharma, Pooja Gokhale Sinha, Vartika Mathur","doi":"10.1007/s00344-024-11406-8","DOIUrl":"https://doi.org/10.1007/s00344-024-11406-8","url":null,"abstract":"<p>The beneficial effects of endophytes on plant growth, development and yield are well known. Modulating plant growth-promoting substances and ameliorating biotic and abiotic stresses are some of the key mechanisms that are deployed by endophytes to facilitate host growth and defence. However, the understanding of the plant’s genome response to their presence is still limited. Therefore, this study provides an insight into the microbiome of <i>B. juncea</i> seeds as well as leaves, and its impact on plant growth and development. It also correlates their presence with the changes in plant. Removal of seed-borne culturable endophytes resulted in trade-off of accelerated growth with decreased biomass. 16S metagenomics revealed that bacterial endophyte diversity and density varied with stage of the plant. We found that 22 endophytic genera including <i>Enterococcus, Halobacteroides, Planktothrix</i> and <i>Streptomyces</i> were observed irrespective of Bavistin treatment and age of the plant. Removal of culturable endophytes also led to downregulation of crucial genes involved in growth, photosynthesis (Photosystem I assembly protein, Photosystem II reaction center protein and Rubisco), transport (nitrate transporter; <i>NRT</i>) and regulation of plant hormones (auxin homeostasis and signalling; <i>CYP83A1</i>) in <i>B. juncea</i>. To the best of our knowledge, this is the first report of the response of plant’ transcriptome to changes in endophyte composition indicating a strong possibility of host gene regulation by the endophytic partner. The exact mechanism of the same needs to be further explored.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"69 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769316","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cold stress and fungal pathogens pose significant challenge to high-altitude agriculture, impeding plant growth and metabolism. Siderophore-producing plant growth-promoting (PGP) rhizobacteria offer a promising solution by enhancing iron uptake and engaging in pathogen biocontrol. The current research aims to investigate the potential of siderophore-producing psychrotrophic bacteria to manage fungal phytopathogens effectively for its possible application as a bio-inoculant. In our search for psychrotrophic PGP bacteria with biocontrol potential, we isolated 13 rhizobacterial morphotypes; among these, AMR01 showed excellent biofertilizer characteristics. Taxonomic analysis elucidated AMR01 as a potentially novel Pseudomonas species. At 10 °C, AMR01 produced 33.23% siderophore unit (PSU), increasing to 55.76 PSU through pH, NH4NO3, and iron concentration optimization. Furthermore, AMR01 exhibited other PGP attributes, including auxin and ammonia production (13.47 µg/ml and 25.08 mg/l), phosphate solubilization (295.1 µg/ml), nitrogen fixation, potassium solubilization, and hydrogen cyanide (HCN) production. Remarkably, AMR01 demonstrated biocontrol potential, inhibiting three phytopathogens. Seed bacterization with AMR01 enhanced the germination of fungus-infected seeds, as evidenced by increased root and shoot length, compared to uninoculated control, conferring protection against fungal infestation. Genome analysis identified genes involved in pyoverdine synthesis and PGP traits in AMR01. The biosynthetic gene cluster associated with siderophore, HCN, and NRPS further supported AMR01 as a potent biocontrol agent. This research underscores the capacity of a novel, Pseudomonas sp., to improve plant growth by aiding in nutrient uptake and protecting against phytopathogens. Physiological and genomic evidence supports the potential of AMR01 as a bio-inoculant for addressing fungal-induced diseases in crops grown in the Indian Himalayan region.
{"title":"Physiological and Genomic Elucidation of Cold-Resilient Rhizobacteria Reveals Plant Growth Promotion by Siderophore Optimization and Enhanced Biocontrol Potential Against Fungal Pathogens","authors":"Pallavi Sharma, Girija Kaushal, Shruti Sinai Borker, Ayush Lepcha, Anil Kumar, Rakshak Kumar","doi":"10.1007/s00344-024-11430-8","DOIUrl":"https://doi.org/10.1007/s00344-024-11430-8","url":null,"abstract":"<p>Cold stress and fungal pathogens pose significant challenge to high-altitude agriculture, impeding plant growth and metabolism. Siderophore-producing plant growth-promoting (PGP) rhizobacteria offer a promising solution by enhancing iron uptake and engaging in pathogen biocontrol. The current research aims to investigate the potential of siderophore-producing psychrotrophic bacteria to manage fungal phytopathogens effectively for its possible application as a bio-inoculant. In our search for psychrotrophic PGP bacteria with biocontrol potential, we isolated 13 rhizobacterial morphotypes; among these, AMR01 showed excellent biofertilizer characteristics. Taxonomic analysis elucidated AMR01 as a potentially novel <i>Pseudomonas</i> species. At 10 °C, AMR01 produced 33.23% siderophore unit (PSU), increasing to 55.76 PSU through pH, NH<sub>4</sub>NO<sub>3</sub>, and iron concentration optimization. Furthermore, AMR01 exhibited other PGP attributes, including auxin and ammonia production (13.47 µg/ml and 25.08 mg/l), phosphate solubilization (295.1 µg/ml), nitrogen fixation, potassium solubilization, and hydrogen cyanide (HCN) production. Remarkably, AMR01 demonstrated biocontrol potential, inhibiting three phytopathogens. Seed bacterization with AMR01 enhanced the germination of fungus-infected seeds, as evidenced by increased root and shoot length, compared to uninoculated control, conferring protection against fungal infestation. Genome analysis identified genes involved in pyoverdine synthesis and PGP traits in AMR01. The biosynthetic gene cluster associated with siderophore, HCN, and NRPS further supported AMR01 as a potent biocontrol agent. This research underscores the capacity of a novel, <i>Pseudomonas</i> sp., to improve plant growth by aiding in nutrient uptake and protecting against phytopathogens. Physiological and genomic evidence supports the potential of AMR01 as a bio-inoculant for addressing fungal-induced diseases in crops grown in the Indian Himalayan region.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"81 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769319","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-23DOI: 10.1007/s00344-024-11425-5
Vimalraj Kantharaj, Nirmal Kumar Ramasamy, Young-Eun Yoon, Keum-Ah Lee, Vikranth Kumar, Hyeonji Choe, Hadjer Chohra, Young-Nam Kim, Yong Bok Lee
Hydroxyurea (HU) is a known suppressor of ribonucleotide reductase enzyme through enhanced hydrogen peroxide (H2O2) production, causing oxidative damage to DNA in plants. Kinetin (KI) has emerged as an important phytohormone in regulating development processes and antioxidant protection effects against environmental stresses. Therefore, this study aimed to investigate the potential and regulating mechanism of KI application on tolerance of Oryza sativa to HU-induced oxidative stress. Three-day-old rice seedlings were grown in 1/2 MS medium for seven days following different treatments: control, HU (1 mM), KI (40 nM), and HU + KI. The results showed that, compared to control, HU treatment significantly reduced the growth (e.g., dry weight and root length: 36% and 48%, respectively) and photosynthetic rate (e.g., Fv/Fm: 31%) and pigments (e.g., chlorophyll and carotenoid: 52% and 67%, respectively), by stimulating oxidative stress (e.g., H2O2) markers and malondialdehyde levels, causing DNA damage and G1/S (growth/synthesis) and G2/M (growth/mitotic) phase arrest on seven-day-old rice seedlings. Meanwhile, the follow-up treatment of KI to the HU stress plants enhanced the growth (14–31%) and photosynthetic (13–29%) parameters by regulating antioxidant enzyme (e.g., catalase, ascorbate peroxidase, peroxidase, and superoxide dismutase) activities as well as abscisic acid, salicylic acid, gibberellic acid, and indole-3-acetic acid hormone contents, coupled with a significant reduction in reactive oxygen species accumulation. Additionally, KI reduced the DNA damage in the plants exposed to HU stress by reducing the relative density of apurinic/apyrimidinic sites, as evidenced by both decrease and increase in transcriptional regulation of genes (e.g., ATM, ATR, PARP, RAD51A2, and RAD51C) involved in DNA damage response and cell cycle progression. Our findings indicate that exogenous application of KI to plants affected by oxidative stress improves the antioxidant defense system and phytohormone homeostasis as well as DNA damage response alleviating G1/S and G2/M arrest, contributing to enhancement of the rice seedling performance.
众所周知,羟基脲(HU)会通过增强过氧化氢(H2O2)的产生来抑制核糖核苷酸还原酶,从而导致植物 DNA 的氧化损伤。动情素(KI)是一种重要的植物激素,可调节植物的生长发育过程,并对环境胁迫具有抗氧化保护作用。因此,本研究旨在探讨施用 KI 对 Oryza sativa 耐受 HU 诱导的氧化胁迫的潜力和调节机制。在 1/2 MS 培养基中培育 3 天大的水稻幼苗 7 天,分别进行不同的处理:对照、HU(1 mM)、KI(40 nM)和 HU + KI。结果表明,与对照组相比,HU 处理显著降低了秧苗的生长(如干重和根长:分别为 36% 和 48%)、光合速率(如 Fv/Fm:31%)和色素(如叶绿素和类胡萝卜素)、通过刺激氧化应激(如 H2O2)标记和丙二醛水平,造成七天龄水稻秧苗 DNA 损伤和 G1/S(生长/合成)和 G2/M(生长/有丝分裂)期停滞,从而降低光合速率(如 Fv/Fm:31%)和色素(如叶绿素和类胡萝卜素:分别为 52% 和 67%)。同时,通过调节抗氧化酶(如过氧化氢酶、抗坏血酸过氧化物酶、过氧化物酶和超氧化物歧化酶)活性以及脱落酸、水杨酸、赤霉素和吲哚-3-乙酸激素含量,以及显著减少活性氧积累,对 HU 胁迫植株进行 KI 后续处理可提高其生长(14-31%)和光合(13-29%)参数。此外,KI 还通过降低嘌呤/近嘧啶位点的相对密度来减少暴露于 HU 胁迫下的植株的 DNA 损伤,这表现在参与 DNA 损伤响应和细胞周期进展的基因(如 ATM、ATR、PARP、RAD51A2 和 RAD51C)转录调控的减少和增加上。我们的研究结果表明,向受氧化胁迫影响的植物外源施用 KI 可改善抗氧化防御系统和植物激素平衡,以及 DNA 损伤响应,缓解 G1/S 和 G2/M 停滞,从而有助于提高水稻秧苗的生长性能。
{"title":"Regulatory Response of Rice Seedlings to Exogenously Applied Kinetin During Oxidative Stress","authors":"Vimalraj Kantharaj, Nirmal Kumar Ramasamy, Young-Eun Yoon, Keum-Ah Lee, Vikranth Kumar, Hyeonji Choe, Hadjer Chohra, Young-Nam Kim, Yong Bok Lee","doi":"10.1007/s00344-024-11425-5","DOIUrl":"https://doi.org/10.1007/s00344-024-11425-5","url":null,"abstract":"<p>Hydroxyurea (HU) is a known suppressor of ribonucleotide reductase enzyme through enhanced hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) production, causing oxidative damage to DNA in plants. Kinetin (KI) has emerged as an important phytohormone in regulating development processes and antioxidant protection effects against environmental stresses. Therefore, this study aimed to investigate the potential and regulating mechanism of KI application on tolerance of <i>Oryza sativa</i> to HU-induced oxidative stress. Three-day-old rice seedlings were grown in 1/2 MS medium for seven days following different treatments: control, HU (1 mM), KI (40 nM), and HU + KI. The results showed that, compared to control, HU treatment significantly reduced the growth (e.g., dry weight and root length: 36% and 48%, respectively) and photosynthetic rate (e.g., Fv/Fm: 31%) and pigments (e.g., chlorophyll and carotenoid: 52% and 67%, respectively), by stimulating oxidative stress (e.g., H<sub>2</sub>O<sub>2</sub>) markers and malondialdehyde levels, causing DNA damage and G1/S (growth/synthesis) and G2/M (growth/mitotic) phase arrest on seven-day-old rice seedlings. Meanwhile, the follow-up treatment of KI to the HU stress plants enhanced the growth (14–31%) and photosynthetic (13–29%) parameters by regulating antioxidant enzyme (e.g., catalase, ascorbate peroxidase, peroxidase, and superoxide dismutase) activities as well as abscisic acid, salicylic acid, gibberellic acid, and indole-3-acetic acid hormone contents, coupled with a significant reduction in reactive oxygen species accumulation. Additionally, KI reduced the DNA damage in the plants exposed to HU stress by reducing the relative density of apurinic/apyrimidinic sites, as evidenced by both decrease and increase in transcriptional regulation of genes (e.g., <i>ATM</i>, <i>ATR</i>, <i>PARP</i>, <i>RAD51A2</i>, and <i>RAD51C</i>) involved in DNA damage response and cell cycle progression. Our findings indicate that exogenous application of KI to plants affected by oxidative stress improves the antioxidant defense system and phytohormone homeostasis as well as DNA damage response alleviating G1/S and G2/M arrest, contributing to enhancement of the rice seedling performance.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"14 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141769318","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-20DOI: 10.1007/s00344-024-11424-6
Santiago Atero-Calvo, Francesco Magro, Giacomo Masetti, Eloy Navarro-León, Juan Jose Rios, Begoña Blasco, Juan Manuel Ruiz
Humic substances (HS) have been defined as a potential plant biostimulant to improve crop yield in a sustainable and environmentally friendly way. Leonardite-suspension concentrate (SC) is a type of HS extracted from lignite that is currently employed to enhance various physiological aspects of plants. However, the different effects between both modes of SC application (root and foliar) are poorly understood, especially on photosynthesis performance. Therefore, this study aimed to investigate the influence of a leonardite-SC-based product (BLACKJAK®), on lettuce growth and photosynthesis efficiency, while comparing both methods of application. For this purpose, four root (R): R1 (0.20 mL/L), R2 (0.40 mL/L), R3 (0.60 mL/L), and R4 (0.80 mL/L), and four foliar: F1 (5.00 mL/L), F2 (7.50 mL/L), F3 (10.00 mL/L), and F4 (12.50 mL/L) BLACKJAK® doses were applied to lettuce plants. Related shoot and root growth parameters, photosynthetic efficiency, and sugar and starch content were assessed in lettuce plants. The results showed that BLACKJAK® improved shoot and root biomass, foliar area, and root length, especially at intermediate doses (R2, R3, F2, and F3), with R3 demonstrating the greatest growth increases. Similarly, the main photosynthetic parameters analyzed (net photosynthetic rate and Rubisco carboxylation efficiency), and the soluble sugars and starch content were improved by the same doses, with R3 showing the best photosynthetic performance. Hence, our study suggests that BLACKJAK® improves lettuce yield and photosynthetic efficiency, particularly with radicular application at R3.
{"title":"Comparative Effects of Root and Foliar Leonardite-Suspension Concentrate Application on Plant Growth and Photosynthetic Efficiency of Lettuce Plants (Lactuca sativa L.)","authors":"Santiago Atero-Calvo, Francesco Magro, Giacomo Masetti, Eloy Navarro-León, Juan Jose Rios, Begoña Blasco, Juan Manuel Ruiz","doi":"10.1007/s00344-024-11424-6","DOIUrl":"https://doi.org/10.1007/s00344-024-11424-6","url":null,"abstract":"<p>Humic substances (HS) have been defined as a potential plant biostimulant to improve crop yield in a sustainable and environmentally friendly way. Leonardite-suspension concentrate (SC) is a type of HS extracted from lignite that is currently employed to enhance various physiological aspects of plants. However, the different effects between both modes of SC application (root and foliar) are poorly understood, especially on photosynthesis performance. Therefore, this study aimed to investigate the influence of a leonardite-SC-based product (BLACKJAK®), on lettuce growth and photosynthesis efficiency, while comparing both methods of application. For this purpose, four root (R): R1 (0.20 mL/L), R2 (0.40 mL/L), R3 (0.60 mL/L), and R4 (0.80 mL/L), and four foliar: F1 (5.00 mL/L), F2 (7.50 mL/L), F3 (10.00 mL/L), and F4 (12.50 mL/L) BLACKJAK® doses were applied to lettuce plants. Related shoot and root growth parameters, photosynthetic efficiency, and sugar and starch content were assessed in lettuce plants. The results showed that BLACKJAK® improved shoot and root biomass, foliar area, and root length, especially at intermediate doses (R2, R3, F2, and F3), with R3 demonstrating the greatest growth increases. Similarly, the main photosynthetic parameters analyzed (net photosynthetic rate and Rubisco carboxylation efficiency), and the soluble sugars and starch content were improved by the same doses, with R3 showing the best photosynthetic performance. Hence, our study suggests that BLACKJAK® improves lettuce yield and photosynthetic efficiency, particularly with radicular application at R3.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"22 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141745453","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-19DOI: 10.1007/s00344-024-11418-4
Weiming Bai, Jingyu Li, Dongtian Zang, Fanting Sun, Yufei Niu, Pengyue Wang, Wenjia You, Nan Li, Peisen Su
Flowering time is critical for the regional adaptation, yield, and reproduction of crop plants. Tyrosine kinase-like (TKL) genes are protein kinases (PKs) that play important roles in various plant processes. However, the functions of only a few TKLs in controlling flowering time in plants have been characterized. As a genetic model system, Brachypodium distachyon has been widely used in the study of gramineous crop species. Here, we identified and characterized the function of the model plant Brachypodium (poaceae) tyrosine kinase-like kinase BdCTR1 in controlling flowering time. BdCTR1 mutation caused earlier flowering compared with wild-type (WT) plants. Transcriptomic analysis revealed 2261 differentially expressed genes (DEGs) related to the circadian rhythm, phytohormone signaling, and flavonoid biosynthesis pathways in Bdctr1 mutants compared with the wild type (WT). Quantitative reverse transcription–polymerase chain reaction (qRT–PCR) revealed that the expression levels of flowering-related genes, including FT, PPD1, CO, and FUL, and ET-related genes, including ETR, MKK, and ERF, were altered in Bdctr1 mutants compared with those in WT plants. Thus, our results show that BdCTR1 plays a role in controlling flowering time by regulating various signaling pathways and contribute to elucidating the molecular mechanisms of PKs in controlling plant flowering.
{"title":"A Tyrosine Kinase-Like Gene BdCTR1 Negatively Regulates Flowering Time in the Model Grass Plant Brachypodium distachyon","authors":"Weiming Bai, Jingyu Li, Dongtian Zang, Fanting Sun, Yufei Niu, Pengyue Wang, Wenjia You, Nan Li, Peisen Su","doi":"10.1007/s00344-024-11418-4","DOIUrl":"https://doi.org/10.1007/s00344-024-11418-4","url":null,"abstract":"<p>Flowering time is critical for the regional adaptation, yield, and reproduction of crop plants. Tyrosine kinase-like (TKL) genes are protein kinases (PKs) that play important roles in various plant processes. However, the functions of only a few TKLs in controlling flowering time in plants have been characterized. As a genetic model system, <i>Brachypodium distachyon</i> has been widely used in the study of gramineous crop species. Here, we identified and characterized the function of the model plant <i>Brachypodium</i> (poaceae) tyrosine kinase-like kinase <i>BdCTR1</i> in controlling flowering time. <i>BdCTR1</i> mutation caused earlier flowering compared with wild-type (WT) plants. Transcriptomic analysis revealed 2261 differentially expressed genes (DEGs) related to the circadian rhythm, phytohormone signaling, and flavonoid biosynthesis pathways in <i>Bdctr1</i> mutants compared with the wild type (WT). Quantitative reverse transcription–polymerase chain reaction (qRT–PCR) revealed that the expression levels of flowering-related genes, including <i>FT</i>, <i>PPD1</i>, <i>CO,</i> and <i>FUL</i>, and ET-related genes, including <i>ETR</i>, <i>MKK</i>, and <i>ERF</i>, were altered in <i>Bdctr1</i> mutants compared with those in WT plants. Thus, our results show that <i>BdCTR1</i> plays a role in controlling flowering time by regulating various signaling pathways and contribute to elucidating the molecular mechanisms of PKs in controlling plant flowering.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"71 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141745247","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-19DOI: 10.1007/s00344-024-11422-8
Qian Zhou, Jilian Wang, Tian Zhang, Mingyuan Li
To adapt to a habitat, halophytes growing at the same saline–alkali levels develop their unique rhizosphere microbial communities, whereas same plant species growing at different saline–alkali levels have different rhizosphere microbial communities. Therefore, understanding the rhizosphere microbial community structure of halophytes in different saline–alkali soils can help explore the microbial diversity and functional potential of important soil microorganisms. In this study, rhizosphere soils of three typical halophytes, namely, Halocnemum strobilaceum, Phragmites communis, and Halostachys caspica, growing at severe, heavy, and moderate saline–alkali soils, respectively, were collected from southern Xinjiang. The community structure and physicochemical properties of fungal species in the total nine rhizosphere soils were investigated. Furthermore, the differences in the fungal community structure, diversity, and ecological functions were analyzed in terms of the extent of saline–alkali level and host plant specificity. Rhizosphere soils in the nine habitats had different physicochemical properties. In terms of host plant type, rhizosphere fungal species diversity and richness were the highest in P. communis, followed by H. caspica and H. strobilaceum. The fungal community diversity and richness followed the pattern of moderate > severe > heavy in different soil salinity and alkali types. Although the three host plants had similar rhizosphere fungal community structures under moderate and heavy saline–alkali conditions, these varied significantly under extremely severe saline–alkali conditions. In total, 315 species were identified across all samples, and they were affiliated with 12 phyla, 37 classes, 69 orders, 138 families, and 244 genera. The number of jointly owned ASVs was 189. In the nine habitats, Ascomycota and Basidiomycota were the dominant phyla, while Alternaria, Neocamarosporium, Filobasidium, and Acremonium were the common dominant genera. A prediction of fungal community functions revealed pathotroph-saprotroph-symbiotroph and saprotrophs to be dominant. At the same saline–alkali level, the functional clustering distance of fungal communities was closer. Factors such as soil organic matter (SOM), available nitrogen (AN), electronic conductivity (EC), and pH contributed to the distribution of microbial communities. This study revealed both similarities and distinctions in the composition of fungal communities within the rhizosphere soils of the three typical halophytes thriving in various saline–alkali habitats. At moderate and heavy saline–alkali levels, the fungal community structures were markedly influenced by the severity of salinity and alkalinity. In extremely severe saline–alkali soils, the host plant type significantly affected the fungal community structure. Ultimately, these findings lay a theoretical foundation for the improvement of soil a
为了适应生境,生长在同一盐碱地的卤叶植物会形成其独特的根圈微生物群落,而生长在不同盐碱地的同一植物物种则具有不同的根圈微生物群落。因此,了解不同盐碱地中卤叶植物的根瘤微生物群落结构有助于探索重要土壤微生物的多样性和功能潜力。本研究从新疆南部采集了生长在重度、中度和重度盐碱地的三种典型盐碱地植物根瘤菌群落土壤,分别为Halocnemum strobilaceum、Phragmites communis和Halostachys caspica。研究了九种根圈土壤中真菌的群落结构和理化性质。此外,还从盐碱程度和寄主植物特异性的角度分析了真菌群落结构、多样性和生态功能的差异。九个生境的根瘤土壤具有不同的理化性质。从寄主植物类型来看,根瘤菌群落的真菌物种多样性和丰富度以 P. communis 最高,其次是 H. caspica 和 H. strobilaceum。真菌群落多样性和丰富度在不同的土壤盐碱度类型中呈现出中度、重度和重度的模式。虽然在中度和重度盐碱条件下,三种寄主植物的根瘤菌群落结构相似,但在极重度盐碱条件下,这些群落结构却有很大差异。所有样本中共鉴定出 315 个物种,它们分别隶属于 12 个门、37 个类、69 个目、138 个科和 244 个属。共同拥有的 ASV 数量为 189 个。在九个生境中,子囊菌门(Ascomycota)和担子菌门(Basidiomycota)是优势菌门,而交替孢属(Alternaria)、新金孢属(Neocamarosporium)、丝孢属(Filobasidium)和cremonium属(Acremonium)是常见的优势属。对真菌群落功能的预测显示,嗜病菌-嗜副真菌-嗜共生真菌和嗜副真菌占优势。在相同的盐碱度下,真菌群落的功能聚类距离更近。土壤有机质(SOM)、可利用氮(AN)、电子电导率(EC)和 pH 值等因素对微生物群落的分布有一定影响。这项研究揭示了生长在不同盐碱地的三种典型卤叶植物根瘤土壤中真菌群落组成的相似性和差异性。在中度和重度盐碱地中,真菌群落结构明显受到盐度和碱度严重程度的影响。在极度严重的盐碱土壤中,寄主植物类型对真菌群落结构有显著影响。这些发现最终为改善盐碱地土壤和提高作物产量奠定了理论基础。
{"title":"Special Fungal Community Structure Formed by Typical Halophytes in the Rhizosphere Soil Under the Synergistic Action of Different Saline and Alkaline Environments","authors":"Qian Zhou, Jilian Wang, Tian Zhang, Mingyuan Li","doi":"10.1007/s00344-024-11422-8","DOIUrl":"https://doi.org/10.1007/s00344-024-11422-8","url":null,"abstract":"<p>To adapt to a habitat, halophytes growing at the same saline–alkali levels develop their unique rhizosphere microbial communities, whereas same plant species growing at different saline–alkali levels have different rhizosphere microbial communities. Therefore, understanding the rhizosphere microbial community structure of halophytes in different saline–alkali soils can help explore the microbial diversity and functional potential of important soil microorganisms. In this study, rhizosphere soils of three typical halophytes, namely, <i>Halocnemum strobilaceum</i>, <i>Phragmites communis</i>, and <i>Halostachys caspica</i>, growing at severe, heavy, and moderate saline–alkali soils, respectively, were collected from southern Xinjiang. The community structure and physicochemical properties of fungal species in the total nine rhizosphere soils were investigated. Furthermore, the differences in the fungal community structure, diversity, and ecological functions were analyzed in terms of the extent of saline–alkali level and host plant specificity. Rhizosphere soils in the nine habitats had different physicochemical properties. In terms of host plant type, rhizosphere fungal species diversity and richness were the highest in <i>P. communis</i>, followed by <i>H. caspica</i> and <i>H. strobilaceum</i>. The fungal community diversity and richness followed the pattern of moderate > severe > heavy in different soil salinity and alkali types. Although the three host plants had similar rhizosphere fungal community structures under moderate and heavy saline–alkali conditions, these varied significantly under extremely severe saline–alkali conditions. In total, 315 species were identified across all samples, and they were affiliated with 12 phyla, 37 classes, 69 orders, 138 families, and 244 genera. The number of jointly owned ASVs was 189. In the nine habitats, Ascomycota and Basidiomycota were the dominant phyla, while <i>Alternaria</i>, <i>Neocamarosporium</i>, <i>Filobasidium</i>, and <i>Acremonium</i> were the common dominant genera. A prediction of fungal community functions revealed pathotroph-saprotroph-symbiotroph and saprotrophs to be dominant. At the same saline–alkali level, the functional clustering distance of fungal communities was closer. Factors such as soil organic matter (SOM), available nitrogen (AN), electronic conductivity (EC), and pH contributed to the distribution of microbial communities. This study revealed both similarities and distinctions in the composition of fungal communities within the rhizosphere soils of the three typical halophytes thriving in various saline–alkali habitats. At moderate and heavy saline–alkali levels, the fungal community structures were markedly influenced by the severity of salinity and alkalinity. In extremely severe saline–alkali soils, the host plant type significantly affected the fungal community structure. Ultimately, these findings lay a theoretical foundation for the improvement of soil a","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"33 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141745248","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-07-18DOI: 10.1007/s00344-024-11420-w
Ziyan Ma, Shuai Yuan, Jingbo Chen, Bing Zhang
As a perennial warm-season turfgrass species with great economic value, bermudagrass (Cynodon dactylon L.) simultaneously has three types of stems: shoot, stolon, and rhizome. However, molecular mechanisms underlying the specialization of the three types of stems remain poorly understood. In this study, the metabolome differences among the three types of stems were analyzed and compared through untargeted metabolomic profiling in combination with transcriptome-wide analyses of the genes participating in the metabolic pathways. A total of 949 metabolites were identified in the three stems, whereas 303, 473, and 330 metabolites were differentially accumulated between shoots and stolons, shoots and rhizomes, and stolons and rhizomes, respectively. Sugars and phenylpropanoids were two enriched categories of metabolites showing preferential accumulation in the three types of stems. Transcriptome and RT-qPCR analyses indicated that gene expression of key enzymes catalyzing the synthesis and transformation of sugars and phenylpropanoids, especially glucose-1-phosphate adenylyltransferase, starch synthase, and phenylalanine ammonia-lyase, were delicately regulated to maintain the sugar-starch and lignin-flavonoid homeostasis in the three stems. The results of this study not only expanded our understanding of metabolism regulation in bermudagrass, but also laid a foundation for molecular mechanism study of stem specialization in this glamorous plant species.
{"title":"Specialization of the Stems into Shoots, Stolons, and Rhizomes in Bermudagrass (Cynodon dactylon L.): Insights from Combined Metabolome and Transcriptome Analyses","authors":"Ziyan Ma, Shuai Yuan, Jingbo Chen, Bing Zhang","doi":"10.1007/s00344-024-11420-w","DOIUrl":"https://doi.org/10.1007/s00344-024-11420-w","url":null,"abstract":"<p>As a perennial warm-season turfgrass species with great economic value, bermudagrass <i>(Cynodon dactylon</i> L.) simultaneously has three types of stems: shoot, stolon, and rhizome. However, molecular mechanisms underlying the specialization of the three types of stems remain poorly understood. In this study, the metabolome differences among the three types of stems were analyzed and compared through untargeted metabolomic profiling in combination with transcriptome-wide analyses of the genes participating in the metabolic pathways. A total of 949 metabolites were identified in the three stems, whereas 303, 473, and 330 metabolites were differentially accumulated between shoots and stolons, shoots and rhizomes, and stolons and rhizomes, respectively. Sugars and phenylpropanoids were two enriched categories of metabolites showing preferential accumulation in the three types of stems. Transcriptome and RT-qPCR analyses indicated that gene expression of key enzymes catalyzing the synthesis and transformation of sugars and phenylpropanoids, especially glucose-1-phosphate adenylyltransferase, starch synthase, and phenylalanine ammonia-lyase, were delicately regulated to maintain the sugar-starch and lignin-flavonoid homeostasis in the three stems. The results of this study not only expanded our understanding of metabolism regulation in bermudagrass, but also laid a foundation for molecular mechanism study of stem specialization in this glamorous plant species.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":"64 1","pages":""},"PeriodicalIF":4.8,"publicationDate":"2024-07-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141745452","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}