Lei Chen, Juan He, Xufeng Wang, Shiru Zhang, Jinkang Pan, Jianxiang Peng, Beixin Mo, Lin Liu
MicroRNA827 (miR827) is functionally conserved among different plant species and displays species-specific characteristics, but the mechanisms by which miR827 regulates phosphate (Pi) starvation tolerance and maize development remain elusive. We found that miR827 selectively targets the Pi transporter genes SPX-MFS1 and SPX-MFS5. miR827 overexpression improved the Pi starvation tolerance, plant architecture and grain yield and quality, whereas miR827 suppression yielded a contrasting phenotype. In addition, we identified a specific long noncoding RNA (lncRNA767) that serves as a direct target and a facilitator of miR827 and can stabilize the SPX-MFS1 and SPX-MFS5 transcripts, leading to their translation inhibition. The orchestrated regulation of SPX-MFS1 and SPX-MFS5 modulates PHR1; 1 and PHR1; 2, which are critical transcription factors in Pi signalling, and thereby affects the expression of downstream Pi starvation-induced genes. Together, these findings demonstrate that miR827, assisted by lncRNA767, enhances SPX-MFS1 and SPX-MFS5 suppression and thus exerts a significant impact on Pi homeostasis and several essential agronomic traits of maize.
{"title":"miR827 orchestrates the regulation of SPX-MFS1 and SPX-MFS5 with the assistance of lncRNA767 to enhance phosphate starvation tolerance and maize development","authors":"Lei Chen, Juan He, Xufeng Wang, Shiru Zhang, Jinkang Pan, Jianxiang Peng, Beixin Mo, Lin Liu","doi":"10.1111/pbi.14469","DOIUrl":"https://doi.org/10.1111/pbi.14469","url":null,"abstract":"MicroRNA827 (miR827) is functionally conserved among different plant species and displays species-specific characteristics, but the mechanisms by which miR827 regulates phosphate (Pi) starvation tolerance and maize development remain elusive. We found that miR827 selectively targets the Pi transporter genes <i>SPX-MFS1</i> and <i>SPX-MFS5</i>. miR827 overexpression improved the Pi starvation tolerance, plant architecture and grain yield and quality, whereas miR827 suppression yielded a contrasting phenotype. In addition, we identified a specific long noncoding RNA (<i>lncRNA767</i>) that serves as a direct target and a facilitator of miR827 and can stabilize the <i>SPX-MFS1</i> and <i>SPX-MFS5</i> transcripts, leading to their translation inhibition. The orchestrated regulation of SPX-MFS1 and SPX-MFS5 modulates PHR1; 1 and PHR1; 2, which are critical transcription factors in Pi signalling, and thereby affects the expression of downstream Pi starvation-induced genes. Together, these findings demonstrate that miR827, assisted by <i>lncRNA767</i>, enhances <i>SPX-MFS1</i> and <i>SPX-MFS5</i> suppression and thus exerts a significant impact on Pi homeostasis and several essential agronomic traits of maize.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"53 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142235490","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The cotton genus comprises both diploid and allotetraploid species, and the diversity in petal colour within this genus offers valuable targets for studying orthologous gene function differentiation and evolution. However, the genetic basis for this diversity in petal colour remains largely unknown. The red petal colour primarily comes from C, G, K, and D genome species, and it is likely that the common ancestor of cotton had red petals. Here, by employing a clone mapping strategy, we mapped the red petal trait to a specific region on chromosome A07 in upland cotton. Genomic comparisons and phylogenetic analyses revealed that the red petal phenotype introgressed from G. bickii. Transcriptome analysis indicated that GhRPRS1, which encodes a glutathione S-transferase, was the causative gene for the red petal colour. Knocking out GhRPRS1 resulted in white petals and the absence of red spots, while overexpression of both genotypes of GhRPRS1 led to red petals. Further analysis suggested that GhRPRS1 played a role in transporting pelargonidin-3-O-glucoside and cyanidin-3-O-glucoside. Promoter activity analysis indicated that variations in the promoter, but not in the gene body of GhRPRS1, have led to different petal colours within the genus. Our findings provide new insights into orthologous gene evolution as well as new strategies for modifying promoters in cotton breeding.
棉花属包括二倍体和异源四倍体物种，该属花瓣颜色的多样性为研究正交基因功能分化和进化提供了宝贵的目标。然而，花瓣颜色多样性的遗传基础在很大程度上仍然未知。红色花瓣主要来自 C、G、K 和 D 基因组物种，棉花的共同祖先很可能具有红色花瓣。在此，我们采用克隆作图策略，将红色花瓣性状绘制到陆地棉 A07 染色体上的一个特定区域。基因组比较和系统进化分析表明，红色花瓣表型是从 G. bickii 传入的。转录组分析表明，编码谷胱甘肽 S-转移酶的 GhRPRS1 是红色花瓣的致病基因。敲除 GhRPRS1 会导致花瓣变白且没有红色斑点，而过表达两种基因型的 GhRPRS1 则会导致花瓣变红。进一步的分析表明，GhRPRS1 在运输鹅掌楸素-3-O-葡萄糖苷和青花素-3-O-葡萄糖苷中发挥作用。启动子活性分析表明，启动子（而非 GhRPRS1 基因体）的变异导致了花瓣属中花瓣颜色的不同。我们的研究结果为同源基因的进化提供了新的视角，也为棉花育种中修改启动子提供了新的策略。
{"title":"Natural variations in the Cis-elements of GhRPRS1 contributing to petal colour diversity in cotton","authors":"Wei Hu, Yanli Chen, Zhenzhen Xu, Linqiang Liu, Da Yan, Miaoyang Liu, Qingdi Yan, Yihao Zhang, Lan Yang, Chenxu Gao, Renju Liu, Wenqiang Qin, Pengfei Miao, Meng Ma, Peng Wang, Babai Gao, Fuguang Li, Zhaoen Yang","doi":"10.1111/pbi.14468","DOIUrl":"https://doi.org/10.1111/pbi.14468","url":null,"abstract":"The cotton genus comprises both diploid and allotetraploid species, and the diversity in petal colour within this genus offers valuable targets for studying orthologous gene function differentiation and evolution. However, the genetic basis for this diversity in petal colour remains largely unknown. The red petal colour primarily comes from C, G, K, and D genome species, and it is likely that the common ancestor of cotton had red petals. Here, by employing a clone mapping strategy, we mapped the red petal trait to a specific region on chromosome A07 in upland cotton. Genomic comparisons and phylogenetic analyses revealed that the red petal phenotype introgressed from <i>G. bickii</i>. Transcriptome analysis indicated that <i>GhRPRS1</i>, which encodes a glutathione S-transferase, was the causative gene for the red petal colour. Knocking out <i>GhRPRS1</i> resulted in white petals and the absence of red spots, while overexpression of both genotypes of <i>GhRPRS1</i> led to red petals. Further analysis suggested that <i>GhRPRS1</i> played a role in transporting pelargonidin-3-O-glucoside and cyanidin-3-O-glucoside. Promoter activity analysis indicated that variations in the promoter, but not in the gene body of <i>GhRPRS1</i>, have led to different petal colours within the genus. Our findings provide new insights into orthologous gene evolution as well as new strategies for modifying promoters in cotton breeding.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"9 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234059","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Marianna Boccia, Kerstin Ploβ, Maritta Kunert, Radhika Keshan, Mustafa Hatam, Veit Grabe, Sarah E. O'Connor, Prashant D. Sonawane
<p>Vitamin D is a lipid-soluble sterol that plays an essential role in human health. Deficiency of this vitamin increases the risk of osteoporosis, hypertension, autoimmune diseases, infectious disease, diabetes and cancer. Vitamin D exists in two major forms: vitamin D<sub>3</sub> (cholecalciferol), mainly found in animal food source, and vitamin D<sub>2</sub> (ergocalciferol), typically present in sundried and ultraviolet-B (UV-B) exposed fungi and yeast (Jäpelt <i>et al</i>., <span>2013</span>). Vitamin D<sub>3</sub> is produced in human skin upon sunlight exposure, where pro-vitamin D<sub>3</sub> (7-dehydrocholesterol; 7-DHC) is converted to vitamin D<sub>3</sub> by UV-B light (290–315 nm). Unfortunately, vitamin D<sub>3</sub> deficiency is common in both children and adults worldwide. Endogenous synthesis of vitamin D<sub>3</sub> in human skin is inhibited by several factors such as melanin presence, sunlight intensity, pollution and geographic location. Therefore, dietary sources are essential for maintaining consistent vitamin D<sub>3</sub> levels. Unfortunately, few dietary sources and supplements naturally contain vitamin D<sub>3</sub> and most of these are animal-based foods (e.g. meat and eggs), which raises concerns about vitamin D<sub>3</sub> levels among those populations that consume low amounts of animal products (Black <i>et al</i>., <span>2017</span>).</p> <p>Plants harbour an enormous reservoir of diverse steroidal molecules and, in principle, could be a source of vitamin D<sub>3</sub>. However, although vitamin D<sub>3</sub> has been identified in some plants and algae, the levels are much lower compared to animal-based sources. The precursor of vitamin D<sub>3</sub>, 7-DHC, is also the immediate precursor for cholesterol biosynthesis in plants (Figure 1a) (Sonawane <i>et al</i>., <span>2017</span>). Since most plants produce cholesterol in very low amounts, 7-DHC levels are low as well. Notably, <i>Solanaceae</i> family members (e.g. tomato and <i>Nicotiana benthamiana</i>) accumulate naturally high levels of cholesterol. In tomato and other <i>Solanum</i> food crops such as potato and eggplant, cholesterol serves as a starting precursor for biosynthesis of defensive steroidal glycoalkaloids (SGAs) (Sonawane <i>et al</i>., <span>2017</span>). Using the recently elucidated cholesterol pathway in plants along with gene editing strategies, it is now possible to engineer high levels of 7-DHC and therefore, vitamin D<sub>3</sub> in plants. Here, we report metabolic engineering approaches to enhance vitamin D<sub>3</sub> production in tomato (<i>Solanum lycopersicum</i>) and <i>N. benthamiana</i> plants.</p> <figure><picture> <source media="(min-width: 1650px)" srcset="/cms/asset/85d61b05-6977-4ef7-89be-4819803e5579/pbi14459-fig-0001-m.jpg"/><img alt="Details are in the caption following the image" data-lg-src="/cms/asset/85d61b05-6977-4ef7-89be-4819803e5579/pbi14459-fig-0001-m.jpg" loading="lazy" src="/cms/asset/a7f4769b-85b3-4d88
{"title":"Metabolic engineering of vitamin D3 in Solanaceae plants","authors":"Marianna Boccia, Kerstin Ploβ, Maritta Kunert, Radhika Keshan, Mustafa Hatam, Veit Grabe, Sarah E. O'Connor, Prashant D. Sonawane","doi":"10.1111/pbi.14459","DOIUrl":"https://doi.org/10.1111/pbi.14459","url":null,"abstract":"<p>Vitamin D is a lipid-soluble sterol that plays an essential role in human health. Deficiency of this vitamin increases the risk of osteoporosis, hypertension, autoimmune diseases, infectious disease, diabetes and cancer. Vitamin D exists in two major forms: vitamin D<sub>3</sub> (cholecalciferol), mainly found in animal food source, and vitamin D<sub>2</sub> (ergocalciferol), typically present in sundried and ultraviolet-B (UV-B) exposed fungi and yeast (Jäpelt <i>et al</i>., <span>2013</span>). Vitamin D<sub>3</sub> is produced in human skin upon sunlight exposure, where pro-vitamin D<sub>3</sub> (7-dehydrocholesterol; 7-DHC) is converted to vitamin D<sub>3</sub> by UV-B light (290–315 nm). Unfortunately, vitamin D<sub>3</sub> deficiency is common in both children and adults worldwide. Endogenous synthesis of vitamin D<sub>3</sub> in human skin is inhibited by several factors such as melanin presence, sunlight intensity, pollution and geographic location. Therefore, dietary sources are essential for maintaining consistent vitamin D<sub>3</sub> levels. Unfortunately, few dietary sources and supplements naturally contain vitamin D<sub>3</sub> and most of these are animal-based foods (e.g. meat and eggs), which raises concerns about vitamin D<sub>3</sub> levels among those populations that consume low amounts of animal products (Black <i>et al</i>., <span>2017</span>).</p>\u0000<p>Plants harbour an enormous reservoir of diverse steroidal molecules and, in principle, could be a source of vitamin D<sub>3</sub>. However, although vitamin D<sub>3</sub> has been identified in some plants and algae, the levels are much lower compared to animal-based sources. The precursor of vitamin D<sub>3</sub>, 7-DHC, is also the immediate precursor for cholesterol biosynthesis in plants (Figure 1a) (Sonawane <i>et al</i>., <span>2017</span>). Since most plants produce cholesterol in very low amounts, 7-DHC levels are low as well. Notably, <i>Solanaceae</i> family members (e.g. tomato and <i>Nicotiana benthamiana</i>) accumulate naturally high levels of cholesterol. In tomato and other <i>Solanum</i> food crops such as potato and eggplant, cholesterol serves as a starting precursor for biosynthesis of defensive steroidal glycoalkaloids (SGAs) (Sonawane <i>et al</i>., <span>2017</span>). Using the recently elucidated cholesterol pathway in plants along with gene editing strategies, it is now possible to engineer high levels of 7-DHC and therefore, vitamin D<sub>3</sub> in plants. Here, we report metabolic engineering approaches to enhance vitamin D<sub>3</sub> production in tomato (<i>Solanum lycopersicum</i>) and <i>N. benthamiana</i> plants.</p>\u0000<figure><picture>\u0000<source media=\"(min-width: 1650px)\" srcset=\"/cms/asset/85d61b05-6977-4ef7-89be-4819803e5579/pbi14459-fig-0001-m.jpg\"/><img alt=\"Details are in the caption following the image\" data-lg-src=\"/cms/asset/85d61b05-6977-4ef7-89be-4819803e5579/pbi14459-fig-0001-m.jpg\" loading=\"lazy\" src=\"/cms/asset/a7f4769b-85b3-4d88","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"115 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234058","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
SummaryVernalization and photoperiod pathways converging at FT1 control the transition to flowering in wheat. Here, we identified a gain‐of‐function mutation in FT‐D1 that results in earlier heading date (HD), and shorter plant height and spike length in the gamma ray‐induced eh1 wheat mutant. Knockout of the wild‐type and overexpression of the mutated FT‐D1 indicate that both alleles are functional to affect HD and plant height. Protein interaction assays demonstrated that the frameshift mutation in FT‐D1eh1 exon 3 led to gain‐of‐function interactions with 14‐3‐3A and FDL6, thereby enabling the formation of florigen activation complex (FAC) and consequently activating a flowering‐related transcriptomic programme. This mutation did not affect FT‐D1eh1 interactions with TaNaKR5 or TaFTIP7, both of which could modulate HD, potentially via mediating FT‐D1 translocation to the shoot apical meristem. Furthermore, the ‘Segment B’ external loop is essential for FT‐D1 interaction with FDL6, while residue Y85 is required for interactions with TaNaKR5 and TaFTIP7. Finally, the flowering regulatory hub gene, ELF5, was identified as the FT‐D1 regulatory target. This study illustrates FT‐D1 function in determining wheat HD with a suite of interaction partners and provides genetic resources for tuning HD in elite wheat lines.
{"title":"A gain‐of‐function mutation at the C‐terminus of FT‐D1 promotes heading by interacting with 14‐3‐3A and FDL6 in wheat","authors":"Yuting Li, Hongchun Xiong, Huijun Guo, Yongdun Xie, Linshu Zhao, Jiayu Gu, Huiyuan Li, Shirong Zhao, Yuping Ding, Chunyun Zhou, Zhengwu Fang, Luxiang Liu","doi":"10.1111/pbi.14474","DOIUrl":"https://doi.org/10.1111/pbi.14474","url":null,"abstract":"SummaryVernalization and photoperiod pathways converging at <jats:italic>FT1</jats:italic> control the transition to flowering in wheat. Here, we identified a gain‐of‐function mutation in <jats:italic>FT‐D1</jats:italic> that results in earlier heading date (HD), and shorter plant height and spike length in the gamma ray‐induced <jats:italic>eh1</jats:italic> wheat mutant. Knockout of the wild‐type and overexpression of the mutated <jats:italic>FT‐D1</jats:italic> indicate that both alleles are functional to affect HD and plant height. Protein interaction assays demonstrated that the frameshift mutation in FT‐D1<jats:sup><jats:italic>eh1</jats:italic></jats:sup> exon 3 led to gain‐of‐function interactions with 14‐3‐3A and FDL6, thereby enabling the formation of florigen activation complex (FAC) and consequently activating a flowering‐related transcriptomic programme. This mutation did not affect <jats:italic>FT‐D1</jats:italic><jats:sup><jats:italic>eh1</jats:italic></jats:sup> interactions with TaNaKR5 or TaFTIP7, both of which could modulate HD, potentially via mediating FT‐D1 translocation to the shoot apical meristem. Furthermore, the ‘Segment B’ external loop is essential for FT‐D1 interaction with FDL6, while residue Y85 is required for interactions with TaNaKR5 and TaFTIP7. Finally, the flowering regulatory hub gene, <jats:italic>ELF5</jats:italic>, was identified as the <jats:italic>FT‐D1</jats:italic> regulatory target. This study illustrates <jats:italic>FT‐D1</jats:italic> function in determining wheat HD with a suite of interaction partners and provides genetic resources for tuning HD in elite wheat lines.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"7 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142233345","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zhiqiang Wang, Yarong Zhao, Minmin Zheng, Shuojun Yu, Yang Gao, Guangtao Zhu, Jian-Kang Zhu, Kai Hua, Zhen Wang
<p>Tomato is the most widely consumed fruit and vegetable crop in the world, serving as an important source of micronutrients in human diet (Zhu <i>et al</i>., <span>2018</span>). The impact of sugar on the taste of tomato fruits is generally estimated by determining their total soluble solids (TSS) accumulation (Kader, <span>2008</span>), therefore, the determination of TSS is responsible for the fruit quality of tomato designed for fresh market. However, domestication has resulted in a decline in fruit taste from wild ancestors to modern tomato cultivars (Tieman <i>et al</i>., <span>2017</span>). To understand the genetic basis causing this decline, we measured the TSS contents in fruits from a population consisting of 46 wild <i>Solanum pimpinellifolium</i> (SP), 94 semi-domesticated <i>S. lycopersicum</i> var. <i>cerasiforme</i> (SLC) and 148 fully domesticated <i>S. lycopersicum</i> var. <i>lycopersicum</i> (SLL) with large natural variations (Figure S1a; Data set S1). We conducted a genome-wide association study (GWAS) for the TSS using this tomato population with a total of 7 632 172 common SNPs (Zhu <i>et al</i>., <span>2018</span>). The <i>P</i>-value of 1.31 × 10<sup>−7</sup> was set as the significance threshold after Bonferroni-adjusted correction. Two significant associations with TSS levels were identified on chromosomes 8 and 9 (Figure 1a). An extracellular invertase encoding gene <i>Lin5</i> (Solyc09g010080) was found from 11 018 to 6892 bp upstream of the leading SNP (SNP<sub>t</sub>, <i>P</i> = 1.10 × 10<sup>−7</sup>) on chromosome 9 (Figure 1b; Data set S2). The Lin5 facilitates the cleavage of sucrose in apoplast, impacting sugar supply from source organs to fruits in tomato. The variation for <i>Brix9-2-5</i> of <i>Lin5</i> resulted in the conversion of asparagine to glutamic acid at position 348 in <i>S. lycopersicum</i>, which was considered to be a major reason for the decrease in enzyme activity and fruit sink strength compared to the green-fruited <i>S. pennellii</i> (Fridman <i>et al</i>., <span>2004</span>). Sequence analysis revealed the variation of <i>Brix9-2-5</i> was not involved in the red-fruited tomato population, while another significant variation SNP2458 residing in <i>Lin5</i> coding region (2458 bp relative to the start codon) was in strong linkage disequilibrium (<i>r</i><sup><i>2</i></sup> = 0.89) with SNP<sub>t</sub>, thus closely associating with TSS levels (Figure 1b; Data set S3). Based on the reference genome, we found that the SNP2458 variation causes a conversion of adenine (A) to guanine (G), resulting in the substitution of asparagine (N) with aspartic acid (D) at position 366 of Lin5 (Figure 1b). All accessions were subsequently classified into two haplotype groups according to the SNP2458 variation. Accessions with alternative <i>Lin5</i><sup><i>2458G</i></sup> belong to haplotype 1 (Hap1) group, whereas genotypes with reference <i>Lin5</i><sup><i>2458A</i></sup> are representatives of Hap2 gr
{"title":"A natural variation contributes to sugar accumulation in fruit during tomato domestication","authors":"Zhiqiang Wang, Yarong Zhao, Minmin Zheng, Shuojun Yu, Yang Gao, Guangtao Zhu, Jian-Kang Zhu, Kai Hua, Zhen Wang","doi":"10.1111/pbi.14471","DOIUrl":"https://doi.org/10.1111/pbi.14471","url":null,"abstract":"<p>Tomato is the most widely consumed fruit and vegetable crop in the world, serving as an important source of micronutrients in human diet (Zhu <i>et al</i>., <span>2018</span>). The impact of sugar on the taste of tomato fruits is generally estimated by determining their total soluble solids (TSS) accumulation (Kader, <span>2008</span>), therefore, the determination of TSS is responsible for the fruit quality of tomato designed for fresh market. However, domestication has resulted in a decline in fruit taste from wild ancestors to modern tomato cultivars (Tieman <i>et al</i>., <span>2017</span>). To understand the genetic basis causing this decline, we measured the TSS contents in fruits from a population consisting of 46 wild <i>Solanum pimpinellifolium</i> (SP), 94 semi-domesticated <i>S. lycopersicum</i> var. <i>cerasiforme</i> (SLC) and 148 fully domesticated <i>S. lycopersicum</i> var. <i>lycopersicum</i> (SLL) with large natural variations (Figure S1a; Data set S1). We conducted a genome-wide association study (GWAS) for the TSS using this tomato population with a total of 7 632 172 common SNPs (Zhu <i>et al</i>., <span>2018</span>). The <i>P</i>-value of 1.31 × 10<sup>−7</sup> was set as the significance threshold after Bonferroni-adjusted correction. Two significant associations with TSS levels were identified on chromosomes 8 and 9 (Figure 1a). An extracellular invertase encoding gene <i>Lin5</i> (Solyc09g010080) was found from 11 018 to 6892 bp upstream of the leading SNP (SNP<sub>t</sub>, <i>P</i> = 1.10 × 10<sup>−7</sup>) on chromosome 9 (Figure 1b; Data set S2). The Lin5 facilitates the cleavage of sucrose in apoplast, impacting sugar supply from source organs to fruits in tomato. The variation for <i>Brix9-2-5</i> of <i>Lin5</i> resulted in the conversion of asparagine to glutamic acid at position 348 in <i>S. lycopersicum</i>, which was considered to be a major reason for the decrease in enzyme activity and fruit sink strength compared to the green-fruited <i>S. pennellii</i> (Fridman <i>et al</i>., <span>2004</span>). Sequence analysis revealed the variation of <i>Brix9-2-5</i> was not involved in the red-fruited tomato population, while another significant variation SNP2458 residing in <i>Lin5</i> coding region (2458 bp relative to the start codon) was in strong linkage disequilibrium (<i>r</i><sup><i>2</i></sup> = 0.89) with SNP<sub>t</sub>, thus closely associating with TSS levels (Figure 1b; Data set S3). Based on the reference genome, we found that the SNP2458 variation causes a conversion of adenine (A) to guanine (G), resulting in the substitution of asparagine (N) with aspartic acid (D) at position 366 of Lin5 (Figure 1b). All accessions were subsequently classified into two haplotype groups according to the SNP2458 variation. Accessions with alternative <i>Lin5</i><sup><i>2458G</i></sup> belong to haplotype 1 (Hap1) group, whereas genotypes with reference <i>Lin5</i><sup><i>2458A</i></sup> are representatives of Hap2 gr","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"27 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142198028","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
<p>Rice (<i>Oryza sativa</i>) is a staple food supply for over half of the global population. Various phytopathogens including viruses pose a significant threat to rice yield and quality. Southern rice black-streaked dwarf virus (SRBSDV), belonged to the genus <i>Fijivirus</i>, family <i>Reoviridae</i>, has become a major virus species leading to substantial crop losses in Asian nations (Zhang <i>et al</i>., <span>2023</span>). Traditional breeding and commercial rice varieties face challenges in achieving viral resistance due to the absence of natural resistance. Therefore, it is crucial to utilize biotechnology methods to create and cultivate resistant germplasm for the prevention and control of viral diseases.</p> <p>Oxygenic photosynthesis is the primary process that converts sunlight into chemical energy in higher plants. The light reaction of photosynthesis is driven by photosystems I and II (PSI and PSII). PSI is a membrane protein complex that enables sunlight-driven transmembrane electron transfer as a component of the photosynthetic machinery (Malavath <i>et al</i>., <span>2018</span>; Varotto <i>et al</i>., <span>2000</span>). As a component of PSI, PsaL is crucial for the formation of PSI trimers, a process likely reliant on the binding of calcium ions to the PsaL subunit. However, the involvement of PsaL in plant growth and immunity remains unclear.</p> <p>Clustered regularly interspaced short palindromic repeats/CRISPR-associated 9 (CRISPR/Cas9) technology have been effectively utilized to create new cultivars from wild species via de novo domestication (Bai <i>et al</i>., <span>2023</span>). In this study, we demonstrate the successful application of CRISPR/Cas9 in rice to create the transgenic lines with superior agronomic traits and resistance to SRBSDV. We firstly found that the expression level of <i>OsPsaL</i> gene was significantly down-regulated following SRBSDV infection (Figure 1a). Then, we generated two independent <i>ospsal-ko</i> mutants (<i>ospsal-1</i> and <i>ospsal-2</i>) via the CRISPR/Cas9 system in the <i>Nipponbare</i> (NIP) background (Figure 1b,c). Subsequently, we used chlorophyll fluorescence to assess the photosynthetic traits of transgenic plants. In contrast to the wild type, the electron transport rate (ETR) and net photosynthetic efficiency (pN) notably increased, while Y(NO), an indicator of unregulated heat dissipation and fluorescence, decreased as light intensity rose in <i>ospsal-ko</i> (Figure 1d–f), indicating that photosynthesis has been enhanced in the mutant. We further constructed overexpressing <i>OsPsaL</i>-transgenic rice named <i>OsPsaL-ox</i> (<i>OsPsaL-3#</i> and <i>OsPsaL-4#</i>) (Figure S1a,b). <i>OsPsaL-ox</i> plants displayed a decreased electron transport rate and net photosynthetic efficiency but exhibited no variance in Y (NO) compared to wild type (Figure S1c–e). Statistical analysis revealed that <i>ospsal-ko</i> has a higher number of tillers, panicles, and grains per plant, b
{"title":"Editing of OsPsaL gene improves both yield and antiviral immunity in rice","authors":"Ruifang Zhang, Hehong Zhang, Lulu Li, Yanjun Li, Kaili Xie, Jianping Chen, Zongtao Sun","doi":"10.1111/pbi.14473","DOIUrl":"https://doi.org/10.1111/pbi.14473","url":null,"abstract":"<p>Rice (<i>Oryza sativa</i>) is a staple food supply for over half of the global population. Various phytopathogens including viruses pose a significant threat to rice yield and quality. Southern rice black-streaked dwarf virus (SRBSDV), belonged to the genus <i>Fijivirus</i>, family <i>Reoviridae</i>, has become a major virus species leading to substantial crop losses in Asian nations (Zhang <i>et al</i>., <span>2023</span>). Traditional breeding and commercial rice varieties face challenges in achieving viral resistance due to the absence of natural resistance. Therefore, it is crucial to utilize biotechnology methods to create and cultivate resistant germplasm for the prevention and control of viral diseases.</p>\u0000<p>Oxygenic photosynthesis is the primary process that converts sunlight into chemical energy in higher plants. The light reaction of photosynthesis is driven by photosystems I and II (PSI and PSII). PSI is a membrane protein complex that enables sunlight-driven transmembrane electron transfer as a component of the photosynthetic machinery (Malavath <i>et al</i>., <span>2018</span>; Varotto <i>et al</i>., <span>2000</span>). As a component of PSI, PsaL is crucial for the formation of PSI trimers, a process likely reliant on the binding of calcium ions to the PsaL subunit. However, the involvement of PsaL in plant growth and immunity remains unclear.</p>\u0000<p>Clustered regularly interspaced short palindromic repeats/CRISPR-associated 9 (CRISPR/Cas9) technology have been effectively utilized to create new cultivars from wild species via de novo domestication (Bai <i>et al</i>., <span>2023</span>). In this study, we demonstrate the successful application of CRISPR/Cas9 in rice to create the transgenic lines with superior agronomic traits and resistance to SRBSDV. We firstly found that the expression level of <i>OsPsaL</i> gene was significantly down-regulated following SRBSDV infection (Figure 1a). Then, we generated two independent <i>ospsal-ko</i> mutants (<i>ospsal-1</i> and <i>ospsal-2</i>) via the CRISPR/Cas9 system in the <i>Nipponbare</i> (NIP) background (Figure 1b,c). Subsequently, we used chlorophyll fluorescence to assess the photosynthetic traits of transgenic plants. In contrast to the wild type, the electron transport rate (ETR) and net photosynthetic efficiency (pN) notably increased, while Y(NO), an indicator of unregulated heat dissipation and fluorescence, decreased as light intensity rose in <i>ospsal-ko</i> (Figure 1d–f), indicating that photosynthesis has been enhanced in the mutant. We further constructed overexpressing <i>OsPsaL</i>-transgenic rice named <i>OsPsaL-ox</i> (<i>OsPsaL-3#</i> and <i>OsPsaL-4#</i>) (Figure S1a,b). <i>OsPsaL-ox</i> plants displayed a decreased electron transport rate and net photosynthetic efficiency but exhibited no variance in Y (NO) compared to wild type (Figure S1c–e). Statistical analysis revealed that <i>ospsal-ko</i> has a higher number of tillers, panicles, and grains per plant, b","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"44 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142198219","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plants offer a promising chassis for the large-scale, cost-effective production of diverse therapeutics, including antimicrobial peptides (AMPs). However, key advances will reduce production costs, including simplifying the downstream processing and purification steps. Here, using Nicotiana benthamiana plants, we present an improved modular design that enables AMPs to be secreted via the endomembrane system and sequestered in an extracellular compartment, the apoplast. Additionally, we translationally fused an AMP to a mutated small ubiquitin-like modifier sequence, thereby enhancing peptide yield and solubilizing the peptide with minimal aggregation and reduced occurrence of necrotic lesions in the plant. This strategy resulted in substantial peptide accumulation, reaching around 2.9 mg AMP per 20 g fresh weight of leaf tissue. Furthermore, the purified AMP demonstrated low collateral toxicity in primary human skin cells, killed pathogenic bacteria by permeabilizing the membrane and exhibited anti-infective efficacy in a preclinical mouse (Mus musculus) model system, reducing bacterial loads by up to three orders of magnitude. A base-case techno-economic analysis demonstrated the economic advantages and scalability of our plant-based platform. We envision that our work can establish plants as efficient bioreactors for producing preclinical-grade AMPs at a commercial scale, with the potential for clinical applications.
{"title":"High-yield, plant-based production of an antimicrobial peptide with potent activity in a mouse model","authors":"Shahid Chaudhary, Zahir Ali, Aarón Pantoja-Angles, Sherin Abdelrahman, Cynthia Olivia Baldelamar Juárez, Gundra Sivakrishna Rao, Pei-Ying Hong, Charlotte Hauser, Magdy Mahfouz","doi":"10.1111/pbi.14460","DOIUrl":"https://doi.org/10.1111/pbi.14460","url":null,"abstract":"Plants offer a promising chassis for the large-scale, cost-effective production of diverse therapeutics, including antimicrobial peptides (AMPs). However, key advances will reduce production costs, including simplifying the downstream processing and purification steps. Here, using <i>Nicotiana benthamiana</i> plants, we present an improved modular design that enables AMPs to be secreted via the endomembrane system and sequestered in an extracellular compartment, the apoplast. Additionally, we translationally fused an AMP to a mutated small ubiquitin-like modifier sequence, thereby enhancing peptide yield and solubilizing the peptide with minimal aggregation and reduced occurrence of necrotic lesions in the plant. This strategy resulted in substantial peptide accumulation, reaching around 2.9 mg AMP per 20 g fresh weight of leaf tissue. Furthermore, the purified AMP demonstrated low collateral toxicity in primary human skin cells, killed pathogenic bacteria by permeabilizing the membrane and exhibited anti-infective efficacy in a preclinical mouse (<i>Mus musculus</i>) model system, reducing bacterial loads by up to three orders of magnitude. A base-case techno-economic analysis demonstrated the economic advantages and scalability of our plant-based platform. We envision that our work can establish plants as efficient bioreactors for producing preclinical-grade AMPs at a commercial scale, with the potential for clinical applications.","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"10 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142171404","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
<p>Gene copy number is crucial for understanding genomic architecture and its implications in plant and animal genetics (Alonge <i>et al</i>., <span>2020</span>; Castagnone-Sereno <i>et al</i>., <span>2019</span>). In agriculture, variations in gene copy number (CNVs) are vital as they affect yield, stress resistance and metabolic capabilities (Yuan <i>et al</i>., <span>2021</span>). Transgenesis, involving the introduction of foreign DNA into plant genomes, has revolutionized agriculture by creating genetically modified (GM) plants with desirable traits. Assessing gene copy numbers in GMOs ensures stability and expression of introduced traits and is crucial for regulatory compliance and biosafety assessments (Liang <i>et al</i>., <span>2022</span>). Evaluating gene copy numbers in transgenic plants is technically challenging due to variability in transgene integration events (Faure, <span>2021</span>). Various techniques like Southern blotting (SB), quantitative real-time PCR (qPCR), digital PCR (dPCR) and paired-end whole-genome sequencing (PE-WGS) have been reported for gene copy number determination (Cusenza <i>et al</i>., <span>2021</span>). However, no systematic comparison of these four methods has been reported, especially concerning PE-WGS.</p> <p>Here, we performed a comparative benchmarking of gene copy number assessment techniques, including SB, qPCR, dPCR and PE-WGS, employing 4 GM crop events (FG72 soybean, 12-5 maize, G6H1 and G281 rice) as examples (Figure 1a; Data S1).</p> <figure><picture> <source media="(min-width: 1650px)" srcset="/cms/asset/800ca9d8-87ce-48cd-b7cf-1f99deca6de1/pbi14466-fig-0001-m.jpg"/><img alt="Details are in the caption following the image" data-lg-src="/cms/asset/800ca9d8-87ce-48cd-b7cf-1f99deca6de1/pbi14466-fig-0001-m.jpg" loading="lazy" src="/cms/asset/dec6a469-300e-43d3-a4bf-08ed5e20ab2a/pbi14466-fig-0001-m.png" title="Details are in the caption following the image"/></picture><figcaption> <div><strong>Figure 1<span style="font-weight:normal"></span></strong><div>Open in figure viewer<i aria-hidden="true"></i><span>PowerPoint</span></div> </div> <div>(a) The workflow of the benchmarking study of gene copy number estimation, the diagrams of exogenous gene cassettes of the tested GM events (FG72, G281, G6H1 and 12-5), and the position of hybrid probes in Southern blotting analysis. (b) Southern blotting analysis of four events with various restriction enzymes. GM, GM event; M, DNA marker; P, positive control; WT, the corresponding recipient line of GM event. (c) The constructed standard curves of qPCR assays employing corresponding plasmid calibrators of exogenous and endogenous genes. (d) Summarizes the copy numbers of transgenes determined from Southern blotting, qPCR, ddPCR and PE-WGS analysis. (e) Advantages and disadvantages of the four methods in transgene copy number evaluation. dPCR, digital PCR; GM, genetically modified; PCR, polymerase chain reaction; PE-WGS, paired-end whole-genome sequencing;
{"title":"Comparative evaluation of gene copy number estimation techniques in genetically modified crops: insights from Southern blotting, qPCR, dPCR and NGS","authors":"Wenting Xu, Jingang Liang, Fan Wang, Litao Yang","doi":"10.1111/pbi.14466","DOIUrl":"https://doi.org/10.1111/pbi.14466","url":null,"abstract":"<p>Gene copy number is crucial for understanding genomic architecture and its implications in plant and animal genetics (Alonge <i>et al</i>., <span>2020</span>; Castagnone-Sereno <i>et al</i>., <span>2019</span>). In agriculture, variations in gene copy number (CNVs) are vital as they affect yield, stress resistance and metabolic capabilities (Yuan <i>et al</i>., <span>2021</span>). Transgenesis, involving the introduction of foreign DNA into plant genomes, has revolutionized agriculture by creating genetically modified (GM) plants with desirable traits. Assessing gene copy numbers in GMOs ensures stability and expression of introduced traits and is crucial for regulatory compliance and biosafety assessments (Liang <i>et al</i>., <span>2022</span>). Evaluating gene copy numbers in transgenic plants is technically challenging due to variability in transgene integration events (Faure, <span>2021</span>). Various techniques like Southern blotting (SB), quantitative real-time PCR (qPCR), digital PCR (dPCR) and paired-end whole-genome sequencing (PE-WGS) have been reported for gene copy number determination (Cusenza <i>et al</i>., <span>2021</span>). However, no systematic comparison of these four methods has been reported, especially concerning PE-WGS.</p>\u0000<p>Here, we performed a comparative benchmarking of gene copy number assessment techniques, including SB, qPCR, dPCR and PE-WGS, employing 4 GM crop events (FG72 soybean, 12-5 maize, G6H1 and G281 rice) as examples (Figure 1a; Data S1).</p>\u0000<figure><picture>\u0000<source media=\"(min-width: 1650px)\" srcset=\"/cms/asset/800ca9d8-87ce-48cd-b7cf-1f99deca6de1/pbi14466-fig-0001-m.jpg\"/><img alt=\"Details are in the caption following the image\" data-lg-src=\"/cms/asset/800ca9d8-87ce-48cd-b7cf-1f99deca6de1/pbi14466-fig-0001-m.jpg\" loading=\"lazy\" src=\"/cms/asset/dec6a469-300e-43d3-a4bf-08ed5e20ab2a/pbi14466-fig-0001-m.png\" title=\"Details are in the caption following the image\"/></picture><figcaption>\u0000<div><strong>Figure 1<span style=\"font-weight:normal\"></span></strong><div>Open in figure viewer<i aria-hidden=\"true\"></i><span>PowerPoint</span></div>\u0000</div>\u0000<div>(a) The workflow of the benchmarking study of gene copy number estimation, the diagrams of exogenous gene cassettes of the tested GM events (FG72, G281, G6H1 and 12-5), and the position of hybrid probes in Southern blotting analysis. (b) Southern blotting analysis of four events with various restriction enzymes. GM, GM event; M, DNA marker; P, positive control; WT, the corresponding recipient line of GM event. (c) The constructed standard curves of qPCR assays employing corresponding plasmid calibrators of exogenous and endogenous genes. (d) Summarizes the copy numbers of transgenes determined from Southern blotting, qPCR, ddPCR and PE-WGS analysis. (e) Advantages and disadvantages of the four methods in transgene copy number evaluation. dPCR, digital PCR; GM, genetically modified; PCR, polymerase chain reaction; PE-WGS, paired-end whole-genome sequencing; ","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"105 1","pages":""},"PeriodicalIF":13.8,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142171405","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Matthew E Dwyer, John E Froehlich, Daniel A Raba, Melissa Borrusch, Linda Danhof, Naveen Sharma, Eric J Young, Federica Brandizzi, Christoph Benning, Cheryl A Kerfeld
{"title":"Towards chloroplastic nanofactories: formation of proteinaceous scaffolds for metabolic engineering.","authors":"Matthew E Dwyer, John E Froehlich, Daniel A Raba, Melissa Borrusch, Linda Danhof, Naveen Sharma, Eric J Young, Federica Brandizzi, Christoph Benning, Cheryl A Kerfeld","doi":"10.1111/pbi.14462","DOIUrl":"https://doi.org/10.1111/pbi.14462","url":null,"abstract":"","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":" ","pages":""},"PeriodicalIF":10.1,"publicationDate":"2024-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142138821","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Eukaryotic translation initiation factors (eIFs) are the primary targets for overcoming RNA virus resistance in plants. In a previous study, we mapped a BjeIF2Bβ from Brassica juncea representing a new class of plant virus resistance genes associated with resistance to Turnip mosaic virus (TuMV). However, the mechanism underlying eIF2Bβ-mediated virus resistance remains unclear. In this study, we discovered that the natural variation of BjeIF2Bβ in the allopolyploid B. juncea was inherited from one of its ancestors, B. rapa. By editing of eIF2Bβ, we were able to confer resistance to TuMV in B. juncea and in its sister species of B. napus. Additionally, we identified an N6-methyladenosine (m6A) demethylation factor, BjALKBH9B, for interaction with BjeIF2Bβ, where BjALKBH9B co-localized with both BjeIF2Bβ and TuMV. Furthermore, BjeIF2Bβ recruits BjALKBH9B to modify the m6A status of TuMV viral coat protein RNA, which lacks the ALKB homologue in its genomic RNA, thereby affecting viral infection. Our findings have applications for improving virus resistance in the Brassicaceae family through natural variation or genome editing of the eIF2Bβ. Moreover, we uncovered a non-canonical translational control of viral mRNA in the host plant.
{"title":"eIF2Bβ confers resistance to Turnip mosaic virus by recruiting ALKBH9B to modify viral RNA methylation","authors":"Tongyun Sha, Zhangping Li, Shirui Xu, Tongbing Su, Jannat Shopan, Xingming Jin, Yueying Deng, Xiaolong Lyu, Zhongyuan Hu, Mingfang Zhang, Jinghua Yang","doi":"10.1111/pbi.14442","DOIUrl":"10.1111/pbi.14442","url":null,"abstract":"<p>Eukaryotic translation initiation factors (<i>eIFs</i>) are the primary targets for overcoming RNA virus resistance in plants. In a previous study, we mapped a <i>BjeIF2Bβ</i> from <i>Brassica juncea</i> representing a new class of plant virus resistance genes associated with resistance to Turnip mosaic virus (TuMV). However, the mechanism underlying eIF2Bβ-mediated virus resistance remains unclear. In this study, we discovered that the natural variation of <i>BjeIF2Bβ</i> in the allopolyploid <i>B. juncea</i> was inherited from one of its ancestors, <i>B. rapa</i>. By editing of <i>eIF2Bβ</i>, we were able to confer resistance to TuMV in <i>B. juncea</i> and in its sister species of <i>B. napus</i>. Additionally, we identified an N<sup>6</sup>-methyladenosine (m<sup>6</sup>A) demethylation factor, BjALKBH9B, for interaction with BjeIF2Bβ, where BjALKBH9B co-localized with both BjeIF2Bβ and TuMV. Furthermore, BjeIF2Bβ recruits BjALKBH9B to modify the m<sup>6</sup>A status of TuMV viral coat protein RNA, which lacks the ALKB homologue in its genomic RNA, thereby affecting viral infection. Our findings have applications for improving virus resistance in the Brassicaceae family through natural variation or genome editing of the <i>eIF2Bβ</i>. Moreover, we uncovered a non-canonical translational control of viral mRNA in the host plant.</p>","PeriodicalId":221,"journal":{"name":"Plant Biotechnology Journal","volume":"22 11","pages":"3205-3217"},"PeriodicalIF":10.1,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/pbi.14442","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142124387","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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