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Cas9-targeted Nanopore sequencing rapidly elucidates the transposition preferences and DNA methylation profiles of mobile elements in plants
Pavel Merkulov, Sofya Gvaramiya, Maxim Dudnikov, Roman Komakhin, Murad Omarov, Alina Kocheshkova, Zakhar Konstantinov, Alexander Soloviev, Gennady Karlov, Mikhail Divashuk and Ilya Kirov
J Integr Plant Biol 2023, 65 (10): 2242-2261.  
DOI: 10.1111/jipb.13555
Abstract (Browse 456)  |   Save
Transposable element insertions (TEIs) are an important source of genomic innovation by contributing to plant adaptation, speciation, and the production of new varieties. The often large, complex plant genomes make identifying TEIs from short reads difficult and expensive. Moreover, rare somatic insertions that reflect mobilome dynamics are difficult to track using short reads. To address these challenges, we combined Cas9-targeted Nanopore sequencing (CANS) with the novel pipeline NanoCasTE to trace both genetically inherited and somatic TEIs in plants. We performed CANS of the EVADÉ (EVD) retrotransposon in wild-type Arabidopsis thaliana and rapidly obtained up to 40×sequence coverage. Analysis of hemizygous T-DNA insertion sites and genetically inherited insertions of the EVD transposon in the ddm1 (decrease in DNA methylation 1) genome uncovered the crucial role of DNA methylation in shaping EVD insertion preference. We also investigated somatic transposition events of the ONSEN transposon family, finding that genes that are downregulated during heat stress are preferentially targeted by ONSENs. Finally, we detected hypomethylation of novel somatic insertions for two ONSENs. CANS and NanoCasTE are effective tools for detecting TEIs and exploring mobilome organization in plants in response to stress and in different genetic backgrounds, as well as screening T-DNA insertion mutants and transgenic plants.
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The basic helix-loop-helix transcription factor gene, OsbHLH38, plays a key role in controlling rice salt tolerance
Fengping Du, Yinxiao Wang, Juan Wang, Yingbo Li, Yue Zhang, Xiuqin Zhao, Jianlong Xu, Zhikang Li, Tianyong Zhao, Wensheng Wang and Binying Fu
J Integr Plant Biol 2023, 65 (8): 1859-1873.  
doi: 10.1111/jipb.13489
Abstract (Browse 425)  |   Save
The plant hormone abscisic acid (ABA) is crucial for plant seed germination and abiotic stress tolerance. However, the association between ABA sensitivity and plant abiotic stress tolerance remains largely unknown. In this study, 436 rice accessions were assessed for their sensitivity to ABA during seed germination. The considerable diversity in ABA sensitivity among rice germplasm accessions was primarily reflected by the differentiation between the Xian (indica) and Geng (japonica) subspecies and between the upland-Geng and lowland-Geng ecotypes. The upland-Geng accessions were most sensitive to ABA. Genome-wide association analyses identified four major quantitative trait loci containing 21 candidate genes associated with ABA sensitivity of which a basic helix-loop-helix transcription factor gene, OsbHLH38, was the most important for ABA sensitivity. Comprehensive functional analyses using knockout and overexpression transgenic lines revealed that OsbHLH38 expression was responsive to multiple abiotic stresses. Overexpression of OsbHLH38 increased seedling salt tolerance, while knockout of OsbHLH38 increased sensitivity to salt stress. A salt-responsive transcription factor, OsDREB2A, interacted with OsbHLH38 and was directly regulated by OsbHLH38. Moreover, OsbHLH38 affected rice abiotic stress tolerance by mediating the expression of a large set of transporter genes of phytohormones, transcription factor genes, and many downstream genes with diverse functions, including photosynthesis, redox homeostasis, and abiotic stress responsiveness. These results demonstrated that OsbHLH38 is a key regulator in plant abiotic stress tolerance.
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Cited: Web of Science(2)
Simple method for transformation and gene editing in medicinal plants
Xuesong Cao, Hongtao Xie, Minglei Song, Lianghui Zhao, Hailiang Liu, Guofu Li and Jian‐Kang Zhu
J Integr Plant Biol 2024, 66 (1): 17-19.  
doi: 10.1111/jipb.13593
Abstract (Browse 404)  |   Save
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TaTIP41 and TaTAP46 positively regulate drought tolerance in wheat by inhibiting PP2A activity
Jianhui Ma, Yuke Geng, Hong Liu, Mengqi Zhang, Shujuan Liu, Chenyang Hao, Jian Hou, Youfu Zhang, Daijing Zhang, Weijun Zhang, Xueyong Zhang and Tian Li
J Integr Plant Biol 2023, 65 (9): 2056-2070.  
DOI: 10.1111/jipb.13542
Abstract (Browse 393)  |   Save
Drought is a major environmental stress limiting global wheat (Triticum aestivum) production. Exploring drought tolerance genes is important for improving drought adaptation in this crop. Here, we cloned and characterized TaTIP41, a novel drought tolerance gene in wheat. TaTIP41 is a putative conserved component of target of rapamycin (TOR) signaling, and the TaTIP41 homoeologs were expressed in response to drought stress and abscisic acid (ABA). The overexpression of TaTIP41 enhanced drought tolerance and the ABA response, including ABA-induced stomatal closure, while its downregulation using RNA interference (RNAi) had the opposite effect. Furthermore, TaTIP41 physically interacted with TaTAP46, another conserved component of TOR signaling. Like TaTIP41, TaTAP46 positively regulated drought tolerance. Furthermore, TaTIP41 and TaTAP46 interacted with type-2A protein phosphatase (PP2A) catalytic subunits, such as TaPP2A-2, and inhibited their enzymatic activities. Silencing TaPP2A-2 improved drought tolerance in wheat. Together, our findings provide new insights into the roles of TaTIP41 and TaTAP46 in the drought tolerance and ABA response in wheat, and their potential application in improving wheat environmental adaptability.
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Cited: Web of Science(1)
GmJAZ3 interacts with GmRR18a and GmMYC2a to regulate seed traits in soybean
Yang Hu, Yue Liu, Jian‐Jun Tao, Long Lu, Zhi‐Hao Jiang, Jun‐Jie Wei, Chun‐Mei Wu, Cui‐Cui Yin, Wei Li, Ying‐Dong Bi, Yong‐Cai Lai, Wei Wei, Wan‐Ke Zhang, Shou‐Yi Chen and Jin‐Song Zhang
J Integr Plant Biol 2023, 65 (8): 1983-2000.  
doi: 10.1111/jipb.13494
Abstract (Browse 378)  |   Save
Seed weight is usually associated with seed size and is one of the important agronomic traits that determine yield. Understanding of seed weight control is limited, especially in soybean plants. Here we show that Glycine max JASMONATE-ZIM DOMAIN 3 (GmJAZ3), a gene identified through gene co-expression network analysis, regulates seed-related traits in soybean. Overexpression of GmJAZ3 promotes seed size/weight and other organ sizes in stable transgenic soybean plants likely by increasing cell proliferation. GmJAZ3 interacted with both G. max RESPONSE REGULATOR 18a (GmRR18a) and GmMYC2a to inhibit their transcriptional activation of cytokinin oxidase gene G. max CYTOKININ OXIDASE 3-4 (GmCKX3-4), which usually affects seed traits. Meanwhile, the GmRR18a binds to the promoter of GmMYC2a and activates GmMYC2a gene expression. In GmJAZ3-overexpressing soybean seeds, the protein contents were increased while the fatty acid contents were reduced compared to those in the control seeds, indicating that the GmJAZ3 affects seed size/weight and compositions. Natural variation in JAZ3 promoter region was further analyzed and Hap3 promoter correlates with higher promoter activity, higher gene expression and higher seed weight. The Hap3 promoter may be selected and fixed during soybean domestication. JAZ3 orthologs from other plants/crops may also control seed size and weight. Taken together, our study reveals a novel molecular module GmJAZ3-GmRR18a/GmMYC2a-GmCKXs for seed size and weight control, providing promising targets during soybean molecular breeding for better seed traits.
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Cited: Web of Science(3)
CRISPR/Cas9-mediated editing of GmTAP1 confers enhanced resistance to Phytophthora sojae in soybean
Tengfei Liu, Jing Ji, Yuanyuan Cheng, Sicong Zhang, Zeru Wang, Kaixuan Duan and Yuanchao Wang
J Integr Plant Biol 2023, 65 (7): 1609-1612.  
doi: 10.1111/jipb.13476
Abstract (Browse 245)  |   Save
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Cited: Web of Science(3)
DIW1 encoding a clade I PP2C phosphatase negatively regulates drought tolerance by de-phosphorylating TaSnRK1.1 in wheat
Jingyi Wang, Chaonan Li, Long Li, Lifeng Gao, Ge Hu, Yanfei Zhang, Matthew P. Reynolds, Xueyong Zhang, Jizeng Jia, Xinguo Mao and Ruilian Jing
J Integr Plant Biol 2023, 65 (8): 1918-1936.  
doi: 10.1111/jipb.13504
Abstract (Browse 245)  |   Save
Drought seriously impacts wheat production (Triticum aestivum L.), while the exploitation and utilization of genes for drought tolerance are insufficient. Leaf wilting is a direct reflection of drought tolerance in plants. Clade A PP2Cs are abscisic acid (ABA) co-receptors playing vital roles in the ABA signaling pathway, regulating drought response. However, the roles of other clade PP2Cs in drought tolerance, especially in wheat, remain largely unknown. Here, we identified a gain-of-function drought-induced wilting 1 (DIW1) gene from the wheat Aikang 58 mutant library by map-based cloning, which encodes a clade I protein phosphatase 2C (TaPP2C158) with enhanced protein phosphatase activity. Phenotypic analysis of overexpression and CRISPR/Cas9 mutant lines demonstrated that DIW1/TaPP2C158 is a negative regulator responsible for drought resistance. We found that TaPP2C158 directly interacts with TaSnRK1.1 and de-phosphorylates it, thus inactivating the TaSnRK1.1–TaAREB3 pathway. TaPP2C158 protein phosphatase activity is negatively correlated with ABA signaling. Association analysis suggested that C-terminal variation of TaPP2C158 changing protein phosphatase activity is highly correlated with the canopy temperature, and seedling survival rate under drought stress. Our data suggest that the favorable allele with lower phosphatase activity of TaPP2C158 has been positively selected in Chinese breeding history. This work benefits us in understanding the molecular mechanism of wheat drought tolerance, and provides elite genetic resources and molecular markers for improving wheat drought tolerance.
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Striking a growth–defense balance: Stress regulators that function in maize development
Shiyi Xie, Hongbing Luo, Wei Huang, Weiwei Jin and Zhaobin Dong
J Integr Plant Biol 2024, 66 (3): 424-442.  
doi: 10.1111/jipb.13570
Abstract (Browse 241)  |   Save
Maize (Zea mays) cultivation is strongly affected by both abiotic and biotic stress, leading to reduced growth and productivity. It has recently become clear that regulators of plant stress responses, including the phytohormones abscisic acid (ABA), ethylene (ET), and jasmonic acid (JA), together with reactive oxygen species (ROS), shape plant growth and development. Beyond their well established functions in stress responses, these molecules play crucial roles in balancing growth and defense, which must be finely tuned to achieve high yields in crops while maintaining some level of defense. In this review, we provide an in-depth analysis of recent research on the developmental functions of stress regulators, focusing specifically on maize. By unraveling the contributions of these regulators to maize development, we present new avenues for enhancing maize cultivation and growth while highlighting the potential risks associated with manipulating stress regulators to enhance grain yields in the face of environmental challenges.
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GSK3 regulates VRN1 to control flowering time in wheat
Guoqing Cui, Danping Li, Lichao Zhang, Chuan Xia, Xiuying Kong and Xu Liu
J Integr Plant Biol 2023, 65 (7): 1605-1608.  
doi: 10.1111/jipb.13507
Abstract (Browse 235)  |   Save
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The F-box protein SHORT PRIMARY ROOT modulates primary root meristem activity by targeting SEUSS-LIKE protein for degradation in rice
Nini Ma, Nian Li, Zhongmao Yu, Chunli Chen, Dao‐Xiu Zhou and Yu Zhao
J Integr Plant Biol 2023, 65 (8): 1937-1949.  
DOI: 10.1111/jipb.13492
Abstract (Browse 225)  |   Save
Root meristem activity is essential for root morphogenesis and adaptation, but the molecular mechanism regulating root meristem activity is not fully understood. Here, we identify an F-box family E3 ubiquitin ligase named SHORT PRIMARY ROOT (SHPR) that regulates primary root (PR) meristem activity and cell proliferation in rice. SHPR loss-of-function mutations impair PR elongation in rice. SHPR is involved in the formation of an SCF complex with the Oryza sativa SKP1-like protein OSK1/20. We show that SHPR interacts with Oryza sativa SEUSS-LIKE (OsSLK) in the nucleus and is required for OsSLK polyubiquitination and degradation by the ubiquitin 26S-proteasome system (UPS). Transgenic plants overexpressing OsSLK display a shorter PR phenotype, which is similar to the SHPR loss-of-function mutants. Genetic analysis suggests that SHPR promotes PR elongation in an OsSLK-dependent manner. Collectively, our study establishes SHPR as an E3 ubiquitin ligase that targets OsSLK for degradation, and uncovers a protein ubiquitination pathway as a mechanism for modulating root meristem activity in rice.
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OsWR2 recruits HDA704 to regulate the deacetylation of H4K8ac in the promoter of OsABI5 in response to drought stress
Yalu Guo, Yiqing Tan, Minghao Qu, Kai Hong, Longjun Zeng, Lei Wang, Chuxiong Zhuang, Qian Qian, Jiang Hu and Guosheng Xiong
J Integr Plant Biol 2023, 65 (7): 1651-1669.  
DOI: 10.1111/jipb.13481
Abstract (Browse 225)  |   Save
Drought stress is a major environmental factor that limits the growth, development, and yield of rice (Oryza sativa L.). Histone deacetylases (HDACs) are involved in the regulation of drought stress responses. HDA704 is an RPD3/HDA1 class HDAC that mediates the deacetylation of H4K8 (lysine 8 of histone H4) for drought tolerance in rice. In this study, we show that plants overexpressing HDA704 (HDA704-OE) are resistant to drought stress and sensitive to abscisic acid (ABA), whereas HDA704 knockout mutant (hda704) plants displayed decreased drought tolerance and ABA sensitivity. Transcriptome analysis revealed that HDA704 regulates the expression of ABA-related genes in response to drought stress. Moreover, HDA704 was recruited by a drought-resistant transcription factor, WAX SYNTHESIS REGULATORY 2 (OsWR2), and co-regulated the expression of the ABA biosynthesis genes NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3), NCED4, and NCED5 under drought stress. HDA704 also repressed the expression of ABA-INSENSITIVE 5 (OsABI5) and DWARF AND SMALL SEED 1 (OsDSS1) by regulating H4K8ac levels in the promoter regions in response to polyethylene glycol 6000 treatment. In agreement, the loss of OsABI5 function increased resistance to dehydration stress in rice. Our results demonstrate that HDA704 is a positive regulator of the drought stress response and offers avenues for improving drought resistance in rice.
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An ARF24-ZmArf2 module influences kernel size in different maize haplotypes
Jie Gao, Long Zhang, Haonan Du, Yongbin Dong, Sihan Zhen, Chen Wang, Qilei Wang, Jingyu Yang, Paifeng Zhang, Xu Zheng and Yuling Li
J Integr Plant Biol 2023, 65 (7): 1767-1781.  
DOI: 10.1111/jipb.13473
Abstract (Browse 224)  |   Save
Members of the ADP-ribosylation factor family, which are GTP-binding proteins, are involved in metabolite transport, cell division, and expansion. Although there has been a significant amount of research on small GTP-binding proteins, their roles and functions in regulating maize kernel size remain elusive. Here, we identified ZmArf2 as a maize ADP-ribosylation factor-like family member that is highly conserved during evolution. Maize zmarf2 mutants showed a characteristic smaller kernel size. Conversely, ZmArf2 overexpression increased maize kernel size. Furthermore, heterologous expression of ZmArf2 dramatically elevated Arabidopsis and yeast growth by promoting cell division. Using expression quantitative trait loci (eQTL) analysis, we determined that ZmArf2 expression levels in various lines were mainly associated with variation at the gene locus. The promoters of ZmArf2 genes could be divided into two types, pS and pL, that were significantly associated with both ZmArf2 expression levels and kernel size. In yeast-one-hybrid screening, maize Auxin Response Factor 24 (ARF24) is directly bound to the ZmArf2 promoter region and negatively regulated ZmArf2 expression. Notably, the pS and pL promoter types each contained an ARF24 binding element: an auxin response element (AuxRE) in pS and an auxin response region (AuxRR) in pL, respectively. ARF24 binding affinity to AuxRR was much higher compared with AuxRE. Overall, our results establish that the small G-protein ZmArf2 positively regulates maize kernel size and reveals the mechanism of its expression regulation.
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The brassinosteroid signaling component SlBZR1 promotes tomato fruit ripening and carotenoid accumulation
Fanliang Meng, Haoran Liu, Songshen Hu, Chengguo Jia, Min Zhang, Songwen Li, Yuanyuan Li, Jiayao Lin, Yue Jian, Mengyu Wang, Zhiyong Shao, Yuanyu Mao, Lihong Liu and Qiaomei Wang
J Integr Plant Biol 2023, 65 (7): 1794-1813.  
doi: 10.1111/jipb.13491
Abstract (Browse 220)  |   Save
The plant hormone ethylene is essential for climacteric fruit ripening, although it is unclear how other phytohormones and their interactions with ethylene might affect fruit ripening. Here, we explored how brassinosteroids (BRs) regulate fruit ripening in tomato (Solanum lycopersicum) and how they interact with ethylene. Exogenous BR treatment and increased endogenous BR contents in tomato plants overexpressing the BR biosynthetic gene SlCYP90B3 promoted ethylene production and fruit ripening. Genetic analysis indicated that the BR signaling regulators Brassinazole-resistant1 (SlBZR1) and BRI1-EMS-suppressor1 (SlBES1) act redundantly in fruit softening. Knocking out SlBZR1 inhibited ripening through transcriptome reprogramming at the onset of ripening. Combined transcriptome deep sequencing and chromatin immunoprecipitation followed by sequencing identified 73 SlBZR1-repressed targets and 203 SlBZR1-induced targets involving major ripening-related genes, suggesting that SlBZR1 positively regulates tomato fruit ripening. SlBZR1 directly targeted several ethylene and carotenoid biosynthetic genes to contribute to the ethylene burst and carotenoid accumulation to ensure normal ripening and quality formation. Furthermore, knock-out of Brassinosteroid-insensitive2 (SlBIN2), a negative regulator of BR signaling upstream of SlBZR1, promoted fruit ripening and carotenoid accumulation. Taken together, our results highlight the role of SlBZR1 as a master regulator of tomato fruit ripening with potential for tomato quality improvement and carotenoid biofortification.
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Cited: Web of Science(2)
The SlWRKY57-SlVQ21/SlVQ16 module regulates salt stress in tomato
Jilin Ma, Chonghua Li, Lulu Sun, Xuechun Ma, Hui Qiao, Wenchao Zhao, Rui Yang, Susheng Song, Shaohui Wang and Huang Huang
J Integr Plant Biol 2023, 65 (11): 2437-2455.  
DOI: 10.1111/jipb.13562
Abstract (Browse 219)  |   Save
Salt stress is a major abiotic stress which severely hinders crop production. However, the regulatory network controlling tomato resistance to salt remains unclear. Here, we found that the tomato WRKY transcription factor WRKY57 acted as a negative regulator in salt stress response by directly attenuating the transcription of salt-responsive genes (SlRD29B and SlDREB2) and an ion homeostasis gene (SlSOS1). We further identified two VQ-motif containing proteins SlVQ16 and SlVQ21 as SlWRKY57-interacting proteins. SlVQ16 positively, while SlVQ21 negatively modulated tomato resistance to salt stress. SlVQ16 and SlVQ21 competitively interacted with SlWRKY57 and antagonistically regulated the transcriptional repression activity of SlWRKY57. Additionally, the SlWRKY57-SlVQ21/SlVQ16 module was involved in the pathway of phytohormone jasmonates (JAs) by interacting with JA repressors JA-ZIM domain (JAZ) proteins. These results provide new insights into how the SlWRKY57-SlVQ21/SlVQ16 module finely tunes tomato salt tolerance.
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The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis
Jian‐Ping An, Hong‐Liang Li, Zhi‐Ying Liu, Da‐Ru Wang, Chun‐Xiang You and Yuepeng Han
J Integr Plant Biol 2023, 65 (9): 2175-2193.  
DOI: 10.1111/jipb.13538
Abstract (Browse 211)  |   Save
PHR1 (PHOSPHATE STARVATION RESPONSE1) plays key roles in the inorganic phosphate (Pi) starvation response and in Pi deficiency-induced anthocyanin biosynthesis in plants. However, the post-translational regulation of PHR1 is unclear, and the molecular basis of PHR1-mediated anthocyanin biosynthesis remains elusive. In this study, we determined that MdPHR1 was essential for Pi deficiency-induced anthocyanin accumulation in apple (Malus×domestica). MdPHR1 interacted with MdWRKY75, a positive regulator of anthocyanin biosynthesis, to enhance the MdWRKY75-activated transcription of MdMYB1, leading to anthocyanin accumulation. In addition, the E3 ubiquitin ligase SEVEN IN ABSENTIA1 (MdSINA1) negatively regulated MdPHR1-promoted anthocyanin biosynthesis via the ubiquitination-mediated degradation of MdPHR1. Moreover, the protein kinase apple BRASSINOSTEROID INSENSITIVE2 (MdBIN2) phosphorylated MdPHR1 and positively regulated MdPHR1-mediated anthocyanin accumulation by attenuating the MdSINA1-mediated ubiquitination degradation of MdPHR1. Taken together, these findings not only demonstrate the regulatory role of MdPHR1 in Pi starvation induced anthocyanin accumulation, but also provide an insight into the post-translational regulation of PHR1.
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Auxin signaling module OsSK41-OsIAA10-OsARF regulates grain yield traits in rice
Fuying Ma, Fan Zhang, Yu Zhu, Dengyong Lan, Peiwen Yan, Ying Wang, Zejun Hu, Xinwei Zhang, Jian Hu, Fuan Niu, Mingyu Liu, Shicong He, Jinhao Cui, Xinyu Yuan, Ying Yan, Shujun Wu, Liming Cao, Hongwu Bian, Jinshui Yang, Zhikang Li and Xiaojin Luo
J Integr Plant Biol 2023, 65 (7): 1753-1766.  
doi: 10.1111/jipb.13484
Abstract (Browse 210)  |   Save
Auxin is an important phytohormone in plants, and auxin signaling pathways in rice play key roles in regulating its growth, development, and productivity. To investigate how rice grain yield traits are regulated by auxin signaling pathways and to facilitate their application in rice improvement, we validated the functional relationships among regulatory genes such as OsIAA10, OsSK41, and OsARF21 that are involved in one of the auxin (OsIAA10) signaling pathways. We assessed the phenotypic effects of these genes on several grain yield traits across two environments using knockout and/or overexpression transgenic lines. Based on the results, we constructed a model that showed how grain yield traits were regulated by OsIAA10 and OsTIR1, OsAFB2, and OsSK41 and OsmiR393 in the OsSK41-OsIAA10-OsARF module and by OsARF21 in the transcriptional regulation of downstream auxin response genes in the OsSK41-OsIAA10-OsARF module. The population genomic analyses revealed rich genetic diversity and the presence of major functional alleles at most of these loci in rice populations. The strong differentiation of many major alleles between Xian/indica and Geng/japonica subspecies and/or among modern varieties and landraces suggested that they contributed to improved productivity during evolution and breeding. We identified several important aspects associated with the genetic and molecular bases of rice grain and yield traits that were regulated by auxin signaling pathways. We also suggested rice auxin response factor (OsARF) activators as candidate target genes for improving specific target traits by overexpression and/or editing subspecies-specific alleles and by searching and pyramiding the ‘best’ gene allelic combinations at multiple regulatory genes in auxin signaling pathways in rice breeding programs.
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Efficient CRISPR/Cas9-mediated genome editing in sheepgrass (Leymus chinensis)
Zhelong Lin, Lei Chen, Shanjie Tang, Mengjie Zhao, Tong Li, Jia You, Changqing You, Boshu Li, Qinghua Zhao, Dongmei Zhang, Jianli Wang, Zhongbao Shen, Xianwei Song, Shuaibin Zhang and Xiaofeng Cao
J Integr Plant Biol 2023, 65 (11): 2416-2420.  
DOI: 10.1111/jipb.13567
Abstract (Browse 209)  |   Save
The lack of genome editing platforms has hampered efforts to study and improve forage crops that can be grown on lands not suited to other crops. Here, we established efficient Agrobacterium-mediated clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated nuclease 9 (Cas9) genome editing in a perennial, stress-tolerant forage grass, sheepgrass (Leymus chinensis). By screening for active single-guide RNAs (sgRNAs), accessions that regenerate well, suitable Agrobacterium strains, and optimal culture media, and co-expressing the morphogenic factor TaWOX5, we achieved 11% transformation and 5.83% editing efficiency in sheepgrass. Knocking out Teosinte Branched1 (TB1) significantly increased tiller number and biomass. This study opens avenues for studying gene function and breeding in sheepgrass.
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OsNAC5 orchestrates OsABI5 to fine-tune cold tolerance in rice
Ruiqing Li, Yue Song, Xueqiang Wang, Chenfan Zheng, Bo Liu, Huali Zhang, Jian Ke, Xuejing Wu, Liquan Wu, Ruifang Yang and Meng Jiang
J Integr Plant Biol 2024, 66 (4): 660-682.  
DOI: 10.1111/jipb.13585
Abstract (Browse 204)  |   Save
Due to its tropical origins, rice (Oryza sativa) is susceptible to cold stress, which poses severe threats to production. OsNAC5, a NAC-type transcription factor, participates in the cold stress response of rice, but the detailed mechanisms remain poorly understood. Here, we demonstrate that OsNAC5 positively regulates cold tolerance at germination and in seedlings by directly activating the expression of ABSCISIC ACID INSENSITIVE 5 (OsABI5). Haplotype analysis indicated that single nucleotide polymorphisms in a NAC-binding site in the OsABI5 promoter are strongly associated with cold tolerance. OsNAC5 also enhanced OsABI5 stability, thus regulating the expression of cold-responsive (COR) genes, enabling fine-tuned control of OsABI5 action for rapid, precise plant responses to cold stress. DNA affinity purification sequencing coupled with transcriptome deep sequencing identified several OsABI5 target genes involved in COR expression, including DEHYDRATION-RESPONSIVE ELEMENT BINDING FACTOR 1A (OsDREB1A), OsMYB20, and PEROXIDASE 70 (OsPRX70). In vivo and in vitro analyses suggested that OsABI5 positively regulates COR gene transcription, with marked COR upregulation in OsNAC5-overexpressing lines and downregulation in osnac5 and/or osabi5 knockout mutants. This study extends our understanding of cold tolerance regulation via OsNAC5 through the OsABI5-CORs transcription module, which may be used to ameliorate cold tolerance in rice via advanced breeding.
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A straight-forward seed production technology system for foxtail millet (Setaria italica)
Wei Zhang, Xiantao Qi, Hui Zhi, Yushuang Ren, Linlin Zhang, Yuanzhu Gao, Yi Sui, Haoshan Zhang, Sha Tang, Guanqing Jia, Chuanxiao Xie, Chuanyin Wu and Xianmin Diao
J Integr Plant Biol 2023, 65 (9): 2023-2035.  
DOI: 10.1111/jipb.13503
Abstract (Browse 200)  |   Save
For autogamous crops, a precondition for using heterosis is to produce sufficient pure male-sterile female parents that can be used to produce hybrid seeds. To date, cytoplasmic male sterility (CMS) and environment-sensitive genic male sterility (EGMS) have been used commercially to exploit heterosis for autogamous species. However, neither CMS nor EGMS has been established for foxtail millet (Setaria italica). Here, we report on the establishment and application of a seed production technology (SPT) system for this crop. First, we established a DsRed-based SPT system, but found that it was unsuitable because it required the use of a fluorescent device for seed sorting. Instead, we constructed an SPT system with de novo betalain biosynthesis as the selection marker. This allowed us to distinguish transgenic seeds with the naked eye, thereby facilitating the identification of SPT maintainer line seeds. In this system, a seed sorter was not required to obtain sufficient seeds. The key point of the strategy is that the seed pool of the SPT maintainer line is propagated by artificial identification and harvesting of male-fertile individuals in the field, and the male-sterile line seed pool for hybrid production is produced and propagated by free pollination of male-sterile plants with the SPT maintainer line. In a field experiment, we obtained 423.96 kg male-sterile line seeds per acre, which is sufficient to plant 700.18 acres of farmland for hybrid seed production or male-sterile line reproduction. Our study therefore describes a powerful tool for hybrid seed production in foxtail millet, and demonstrates how the SPT system can be used for a small-grained crop with high reproduction efficiency.
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Cited: Web of Science(2)
Differential SW16.1 allelic effects and genetic backgrounds contributed to increased seed weight after soybean domestication
Xianlian Chen, Cheng Liu, Pengfei Guo, Xiaoshuai Hao, Yongpeng Pan, Kai Zhang, Wusheng Liu, Lizhi Zhao, Wei Luo, Jianbo He, Yanzhu Su, Ting Jin, Fenfen Jiang, Si Wang, Fangdong Liu, Rongzhou Xie, Changgen Zhen, Wei Han, Guangnan Xing, Wubin Wang, Shancen Zhao, Yan Li and Junyi Gai
J Integr Plant Biol 2023, 65 (7): 1734-1752.  
doi: 10.1111/jipb.13480
Abstract (Browse 200)  |   Save
Although seed weight has increased following domestication from wild soybean (Glycine soja) to cultivated soybean (Glycine max), the genetic basis underlying this change is unclear. Using mapping populations derived from chromosome segment substitution lines of wild soybean, we identified SW16.1 as the causative gene underlying a major quantitative trait locus controlling seed weight. SW16.1 encodes a nucleus-localized LIM domain-containing protein. Importantly, the GsSW16.1 allele from wild soybean accession N24852 had a negative effect on seed weight, whereas the GmSW16.1 allele from cultivar NN1138-2 had a positive effect. Gene expression network analysis, reverse-transcription quantitative polymerase chain reaction, and promoter-luciferase reporter transient expression assays suggested that SW16.1 regulates the transcription of MT4, a positive regulator of seed weight. The natural variations in SW16.1 and other known seed weight genes were analyzed in soybean germplasm. The SW16.1 polymorphism was associated with seed weight in 247 soybean accessions, showing much higher frequency of positive-effect alleles in cultivated soybean than in wild soybean. Interestingly, gene allele matrix analysis of the known seed weight genes revealed that G. max has lost 38.5% of the G. soja alleles and that most of the lost alleles had negative effects on seed weight. Our results suggest that eliminating negative alleles from G. soja led to a higher frequency of positive alleles and changed genetic backgrounds in G. max, which contributed to larger seeds in cultivated soybean after domestication from wild soybean. Our findings provide new insights regarding soybean domestication and should assist current soybean breeding programs.
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Cited: Web of Science(1)
MaBEL1 regulates banana fruit ripening by activating cell wall and starch degradation-related genes
Zunyang Song, Xiaoyang Zhu, Xiuhua Lai, Hangcong Chen, Lihua Wang, Yulin Yao, Weixin Chen and Xueping Li
J Integr Plant Biol 2023, 65 (9): 2036-2055.  
doi: 10.1111/jipb.13506
Abstract (Browse 198)  |   Save
Banana is a typical subtropical fruit, sensitive to chilling injuries and prone to softening disorder. However, the underlying regulatory mechanisms of the softening disorder caused by cold stress remain obscure. Herein, we found that BEL1-LIKE HOMEODOMAIN transcription factor 1 (MaBEL1) and its associated proteins regulate the fruit softening and ripening process. The transcript and protein levels of MaBEL1 were up-regulated with fruit ripening but severely repressed by the chilling stress. Moreover, the MaBEL1 protein interacted directly with the promoters of the cell wall and starch degradation-related genes, such as MaAMY3, MaXYL32, and MaEXP-A8. The transient overexpression of MaBEL1 alleviated fruit chilling injury and ripening disorder caused by cold stress and promoted fruit softening and ripening of “Fenjiao” banana by inducing ethylene production and starch and cell wall degradation. The accelerated ripening was also validated by the ectopic overexpression in tomatoes. Conversely, MaBEL1-silencing aggravated the chilling injury and ripening disorder and repressed fruit softening and ripening by inhibiting ethylene production and starch and cell wall degradation. MaABI5-like and MaEBF1, the two positive regulators of the fruit softening process, interacted with MaBEL1 to enhance the promoter activity of the starch and cell wall degradation-related genes. Moreover, the F-box protein MaEBF1 does not modulate the degradation of MaBEL1, which regulates the transcription of MaABI5-like protein. Overall, we report a novel MaBEL1-MaEBF1-MaABI5-like complex system that mediates the fruit softening and ripening disorder in “Fenjiao” bananas caused by cold stress.
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Cited: Web of Science(1)
The transcription factor NAC102 confers cadmium tolerance by regulating WAKL11 expression and cell wall pectin metabolism in Arabidopsis
Guang Hao Han, Ru Nan Huang, Li Hong Hong, Jia Xi Xu, Yi Guo Hong, Yu Huan Wu and Wei Wei Chen
J Integr Plant Biol 2023, 65 (10): 2262-2278.  
DOI: 10.1111/jipb.13557
Abstract (Browse 197)  |   Save
Cadmium (Cd) toxicity severely limits plant growth and development. Moreover, Cd accumulation in vegetables, fruits, and food crops poses health risks to animals and humans. Although the root cell wall has been implicated in Cd stress in plants, whether Cd binding by cell wall polysaccharides contributes to tolerance remains controversial, and the mechanism underlying transcriptional regulation of cell wall polysaccharide biosynthesis in response to Cd stress is unknown. Here, we functionally characterized an Arabidopsis thaliana NAC-type transcription factor, NAC102, revealing its role in Cd stress responses. Cd stress rapidly induced accumulation of NAC102.1, the major transcript encoding functional NAC102, especially in the root apex. Compared to wild type (WT) plants, a nac102 mutant exhibited enhanced Cd sensitivity, whereas NAC102.1-overexpressing plants displayed the opposite phenotype. Furthermore, NAC102 localizes to the nucleus, binds directly to the promoter of WALL-ASSOCIATED KINASE-LIKE PROTEIN11 (WAKL11), and induces transcription, thereby facilitating pectin degradation and decreasing Cd binding by pectin. Moreover, WAKL11 overexpression restored Cd tolerance in nac102 mutants to the WT levels, which was correlated with a lower pectin content and lower levels of pectin-bound Cd. Taken together, our work shows that the NAC102-WAKL11 module regulates cell wall pectin metabolism and Cd binding, thus conferring Cd tolerance in Arabidopsis.
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Artificial evolution of OsEPSPS through an improved dual cytosine and adenine base editor generated a novel allele conferring rice glyphosate tolerance
Chen Zhang, Xue Zhong, Shaoya Li, Lei Yan, Jingying Li, Yubing He, Yong Lin, Yangjun Zhang and Lanqin Xia
J Integr Plant Biol 2023, 65 (9): 2194-2203.  
doi: 10.1111/jipb.13543
Abstract (Browse 195)  |   Save
Exploiting novel endogenous glyphosate-tolerant alleles is highly desirable and has promising potential for weed control in rice breeding. Here, through fusions of different effective cytosine and adenine deaminases with nCas9-NG, we engineered an effective surrogate two-component composite base editing system, STCBE-2, with improved C-to-T and A-to-G base editing efficiency and expanded the editing window. Furthermore, we targeted a rice endogenous OsEPSPS gene for artificial evolution through STCBE-2-mediated near-saturated mutagenesis. After hygromycin and glyphosate selection, we identified a novel OsEPSPS allele with an Asp-213-Asn (D213N) mutation (OsEPSPS-D213N) in the predicted glyphosate-binding domain, which conferred rice plants reliable glyphosate tolerance and had not been reported or applied in rice breeding. Collectively, we developed a novel dual base editor which will be valuable for artificial evolution of important genes in crops. And the novel glyphosate-tolerant rice germplasm generated in this study will benefit weeds management in rice paddy fields.
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Cell type-specific proteomics uncovers a RAF15-SnRK2.6/OST1 kinase cascade in guard cells
Hongliang Wang, Yubei Wang, Tian Sang, Zhen Lin, Rongxia Li, Weiwei Ren, Xin Shen, Bing Zhao, Xiao Wang, Xuebin Zhang, Shaoqun Zhou, Shaojun Dai, Honghong Hu, Chun‐Peng Song and Pengcheng Wang
J Integr Plant Biol 2023, 65 (9): 2122-2137.  
doi: 10.1111/jipb.13536
Abstract (Browse 194)  |   Save
Multicellular organisms such as plants contain various cell types with specialized functions. Analyzing the characteristics of each cell type reveals specific cell functions and enhances our understanding of organization and function at the organismal level. Guard cells (GCs) are specialized epidermal cells that regulate the movement of the stomata and gaseous exchange, and provide a model genetic system for analyzing cell fate, signaling, and function. Several proteomics analyses of GC are available, but these are limited in depth. Here we used enzymatic isolation and flow cytometry to enrich GC and mesophyll cell protoplasts and perform in-depth proteomics in these two major cell types in Arabidopsis leaves. We identified approximately 3,000 proteins not previously found in the GC proteome and more than 600 proteins that may be specific to GC. The depth of our proteomics enabled us to uncover a guard cell-specific kinase cascade whereby Raf15 and Snf1-related kinase2.6 (SnRK2.6)/OST1(open stomata 1) mediate abscisic acid (ABA)-induced stomatal closure. RAF15 directly phosphorylated SnRK2.6/OST1 at the conserved Ser175 residue in its activation loop and was sufficient to reactivate the inactive form of SnRK2.6/OST1. ABA-triggered SnRK2.6/OST1 activation and stomatal closure was impaired in raf15 mutants. We also showed enrichment of enzymes and flavone metabolism in GC, and consistent, dramatic accumulation of flavone metabolites. Our study answers the long-standing question of how ABA activates SnRK2.6/OST1 in GCs and represents a resource potentially providing further insights into the molecular basis of GC and mesophyll cell development, metabolism, structure, and function.
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Fine-tuning brassinosteroid biosynthesis via 3′UTR-dependent decay of CPD mRNA modulates wood formation in Populus
Dian Wang, Xiaoning Hao, Li Xu, Mengyan Zhao, Congpeng Wang, Xihao Yu, Yingzhen Kong, Mengzhu Lu, Gongke Zhou, Guohua Chai and Xianfeng Tang
J Integr Plant Biol 2023, 65 (8): 1852-1858.  
doi: 10.1111/jipb.13509
Abstract (Browse 193)  |   Save
Brassinosteroids (BRs) are plant hormones that regulate wood formation in trees. Currently, little is known about the post-transcriptional regulation of BR synthesis. Here, we show that during wood formation, fine-tuning BR synthesis requires 3′UTR-dependent decay of Populus CONSTITUTIVE PHOTOMORPHOGENIC DWARF 1 (PdCPD1). Overexpression of PdCPD1 or its 3′ UTR fragment resulted in a significant increase of BR levels and inhibited secondary growth. In contrast, transgenic poplars repressing PdCPD1 3′ UTR expression displayed moderate levels of BR and promoted wood formation. We show that the Populus GLYCINE-RICH RNA-BINDING PROTEIN 1 (PdGRP1) directly binds to a GU-rich element in 3′ UTR of PdCPD1, leading to its mRNA decay. We thus provide a post-transcriptional mechanism underlying BRs synthesis during wood formation, which may be useful for genetic manipulation of wood biomass in trees.
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Zinc-finger protein GmZF351 improves both salt and drought stress tolerance in soybean
Wei Wei, Long Lu, Xiao‐Hua Bian, Qing‐Tian Li, Jia‐Qi Han, Jian‐Jun Tao, Cui‐Cui Yin, Yong‐Cai Lai, Wei Li, Ying‐Dong Bi, Wei‐Qun Man, Shou‐Yi Chen, Jin‐Song Zhang and Wan‐Ke Zhang
J Integr Plant Biol 2023, 65 (7): 1636-1650.  
doi: 10.1111/jipb.13474
Abstract (Browse 193)  |   Save
Abiotic stress is one of the most important factors reducing soybean yield. It is essential to identify regulatory factors contributing to stress responses. A previous study found that the tandem CCCH zinc-finger protein GmZF351 is an oil level regulator. In this study, we discovered that the GmZF351 gene is induced by stress and that the overexpression of GmZF351 confers stress tolerance to transgenic soybean. GmZF351 directly regulates the expression of GmCIPK9 and GmSnRK, leading to stomata closing, by binding to their promoter regions, which carry two CT(G/C)(T/A)AA elements. Stress induction of GmZF351 is mediated through reduction in the H3K27me3 level at the GmZF351 locus. Two JMJ30-demethylase-like genes, GmJMJ30-1 and GmJMJ30-2, are involved in this demethylation process. Overexpression of GmJMJ30-1/2 in transgenic hairy roots enhances GmZF351 expression mediated by histone demethylation and confers stress tolerance to soybean. Yield-related agronomic traits were evaluated in stable GmZF351-transgenic plants under mild drought stress conditions. Our study reveals a new mode of GmJMJ30-GmZF351 action in stress tolerance, in addition to that of GmZF351 in oil accumulation. Manipulation of the components in this pathway is expected to improve soybean traits and adaptation under unfavorable environments.
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Cited: Web of Science(4)
The kinase OsSK41/OsGSK5 negatively regulates amylose content in rice endosperm by affecting the interaction between OsEBP89 and OsBP5
Zejun Hu, Fuan Niu, Peiwen Yan, Kai Wang, Lixia Zhang, Ying Yan, Yu Zhu, Shiqing Dong, Fuying Ma, Dengyong Lan, Siwen Liu, Xiaoyun Xin, Ying Wang, Jinshui Yang, Liming Cao, Shujun Wu and Xiaojin Luo
J Integr Plant Biol 2023, 65 (7): 1782-1793.  
doi: 10.1111/jipb.13488
Abstract (Browse 192)  |   Save
Amylose content (AC) is the main factor determining the palatability, viscosity, transparency, and digestibility of rice (Oryza sativa) grains. AC in rice grains is mainly controlled by different alleles of the Waxy (Wx) gene. The AP2/EREBP transcription factor OsEBP89 interacts with the MYC-like protein OsBP5 to synergistically regulate the expression of Wx. Here, we determined that the GLYCOGEN SYNTHASE KINASE 5 (OsGSK5, also named SHAGGY-like kinase 41 [OsSK41]) inhibits the transcriptional activation activity of OsEBP89 in rice grains during amylose biosynthesis. The loss of OsSK41 function enhanced Wx expression and increased AC in rice grains. By contrast, the loss of function of OsEBP89 reduced Wx expression and decreased AC in rice grains. OsSK41 interacts with OsEBP89 and phosphorylates four of its sites (Thr-28, Thr-30, Ser-238, and Thr-257), which makes OsEBP89 unstable and attenuates its interaction with OsBP5. Wx promoter activity was relatively weak when regulated by the phosphomimic variant OsEBP89E–OsBP5 but relatively strong when regulated by the nonphosphorylatable variant OsEBP89A–OsBP5. Therefore, OsSK41-mediated phosphorylation of OsEBP89 represents an additional layer of complexity in the regulation of amylose biosynthesis during rice grain development. In addition, our findings provide four possible sites for regulating rice grain AC via precise gene editing.
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RALF22 promotes plant immunity and amplifies the Pep3 immune signal
Yu-Han He, Song-Yu Chen, Xing-Yan Chen, You-Ping Xu, Yan Liang and Xin-Zhong Cai
J Integr Plant Biol 2023, 65 (11): 2519-2534.  
DOI: 10.1111/jipb.13566
Abstract (Browse 188)  |   Save
Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen-associated molecular pattern (PAMP)-triggered immunity via suppressing PAMP-induced complex formation between the pattern recognition receptor (PRR) and its co-receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)-dependent manner. LORELEI (LRE)-like glycosylphosphatidylinositol (GPI)-anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22-elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22-elicited ROS production and resistance against S. sclerotiorum, demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3-induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3-induced immune signal in a FER-dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection.
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Cited: Web of Science(1)
NIGT1 represses plant growth and mitigates phosphate starvation signaling to balance the growth response tradeoff in rice
Yuxin Zhang, Qianqian Zhang, Meina Guo, Xueqing Wang, Tianjie Li, Qingyu Wu, Lihui Li, Keke Yi and Wenyuan Ruan
J Integr Plant Biol 2023, 65 (8): 1874-1889.  
doi: 10.1111/jipb.13496
Abstract (Browse 181)  |   Save
Inorganic phosphate (Pi) availability is an important factor which affects the growth and yield of crops, thus an appropriate and effective response to Pi fluctuation is critical. However, how crops orchestrate Pi signaling and growth under Pi starvation conditions to optimize the growth defense tradeoff remains unclear. Here we show that a Pi starvation-induced transcription factor NIGT1 (NITRATE-INDUCIBLE GARP-TYPE TRANSCRIPTIONAL REPRESSOR 1) controls plant growth and prevents a hyper-response to Pi starvation by directly repressing the expression of growth-related and Pi-signaling genes to achieve a balance between growth and response under a varying Pi environment. NIGT1 directly binds to the promoters of Pi starvation signaling marker genes, like IPS1, miR827, and SPX2, under Pi-deficient conditions to mitigate the Pi-starvation responsive (PSR). It also directly represses the expression of vacuolar Pi efflux transporter genes VPE1/2 to regulate plant Pi homeostasis. We further demonstrate that NIGT1 constrains shoot growth by repressing the expression of growth-related regulatory genes, including brassinolide signal transduction master regulator BZR1, cell division regulator CYCB1;1, and DNA replication regulator PSF3. Our findings reveal the function of NIGT1 in orchestrating plant growth and Pi starvation signaling, and also provide evidence that NIGT1 acts as a safeguard to avoid hyper-response during Pi starvation stress in rice.
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Plastid KEA-type cation/H+ antiporters are required for vacuolar protein trafficking in Arabidopsis
Xiao Zhang, Lu Wang, Ting Pan, Xuexia Wu, Jinbo Shen, Liwen Jiang, Hiromi Tajima, Eduardo Blumwald and Quan‐Sheng Qiu
J Integr Plant Biol 2023, 65 (9): 2157-2174.  
DOI: 10.1111/jipb.13537
Abstract (Browse 180)  |   Save
Arabidopsis plastid antiporters KEA1 and KEA2 are critical for plastid development, photosynthetic efficiency, and plant development. Here, we show that KEA1 and KEA2 are involved in vacuolar protein trafficking. Genetic analyses found that the kea1 kea2 mutants had short siliques, small seeds, and short seedlings. Molecular and biochemical assays showed that seed storage proteins were missorted out of the cell and the precursor proteins were accumulated in kea1 kea2. Protein storage vacuoles (PSVs) were smaller in kea1 kea2. Further analyses showed that endosomal trafficking in kea1 kea2 was compromised. Vacuolar sorting receptor 1 (VSR1) subcellular localizations, VSR–cargo interactions, and p24 distribution on the endoplasmic reticulum (ER) and Golgi apparatus were affected in kea1 kea2. Moreover, plastid stromule growth was reduced and plastid association with the endomembrane compartments was disrupted in kea1 kea2. Stromule growth was regulated by the cellular pH and K+ homeostasis maintained by KEA1 and KEA2. The organellar pH along the trafficking pathway was altered in kea1 kea2. Overall, KEA1 and KEA2 regulate vacuolar trafficking by controlling the function of plastid stromules via adjusting pH and K+ homeostasis.
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A cell wall invertase modulates resistance to fusarium crown rot and sharp eyespot in common wheat
Guoguo Lv, Yixiao Zhang, Lin Ma, Xiangning Yan, Mingjie Yuan, Jianhui Chen, Yongzhen Cheng, Xi Yang, Qi Qiao, Leilei Zhang, Mohsin Niaz, Xiaonan Sun, Qijun Zhang, Shaobin Zhong and Feng Chen
J Integr Plant Biol 2023, 65 (7): 1814-1825.  
DOI: 10.1111/jipb.13478
Abstract (Browse 179)  |   Save
Fusarium crown rot (FCR) and sharp eyespot (SE) are serious soil-borne diseases in wheat and its relatives that have been reported to cause wheat yield losses in many areas. In this study, the expression of a cell wall invertase gene, TaCWI-B1, was identified to be associated with FCR resistance through a combination of bulk segregant RNA sequencing and genome resequencing in a recombinant inbred line population. Two bi-parental populations were developed to further verify TaCWI-B1 association with FCR resistance. Overexpression lines and ethyl methanesulfonate (EMS) mutants revealed TaCWI-B1 positively regulating FCR resistance. Determination of cell wall thickness and components showed that the TaCWI-B1-overexpression lines exhibited considerably increased thickness and pectin and cellulose contents. Furthermore, we found that TaCWI-B1 directly interacted with an alpha-galactosidase (TaGAL). EMS mutants showed that TaGAL negatively modulated FCR resistance. The expression of TaGAL is negatively correlated with TaCWI-B1 levels, thus may reduce mannan degradation in the cell wall, consequently leading to thickening of the cell wall. Additionally, TaCWI-B1-overexpression lines and TaGAL mutants showed higher resistance to SE; however, TaCWI-B1 mutants were more susceptible to SE than controls. This study provides insights into a FCR and SE resistance gene to combat soil-borne diseases in common wheat.
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Natural variation of GmFATA1B regulates seed oil content and composition in soybean
Zhandong Cai, Peiqi Xian, Yanbo Cheng, Yuan Yang, Yakun Zhang, Zihang He, Chuwen Xiong, Zhibin Guo, Zhicheng Chen, Huiqian Jiang, Qibin Ma, Hai Nian and Liangfa Ge
J Integr Plant Biol 2023, 65 (10): 2368-2379.  
DOI: 10.1111/jipb.13561
Abstract (Browse 178)  |   Save
Soybean (Glycine max) produces seeds that are rich in unsaturated fatty acids and is an important oilseed crop worldwide. Seed oil content and composition largely determine the economic value of soybean. Due to natural genetic variation, seed oil content varies substantially across soybean cultivars. Although much progress has been made in elucidating the genetic trajectory underlying fatty acid metabolism and oil biosynthesis in plants, the causal genes for many quantitative trait loci (QTLs) regulating seed oil content in soybean remain to be revealed. In this study, we identified GmFATA1B as the gene underlying a QTL that regulates seed oil content and composition, as well as seed size in soybean. Nine extra amino acids in the conserved region of GmFATA1B impair its function as a fatty acyl–acyl carrier protein thioesterase, thereby affecting seed oil content and composition. Heterogeneously overexpressing the functional GmFATA1B allele in Arabidopsis thaliana increased both the total oil content and the oleic acid and linoleic acid contents of seeds. Our findings uncover a previously unknown locus underlying variation in seed oil content in soybean and lay the foundation for improving seed oil content and composition in soybean.
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The salt-activated CBF1/CBF2/CBF3-GALS1 module fine-tunes galactan-induced salt hypersensitivity in Arabidopsis
Jingwei Yan, Ya Liu, Jiawen Yan, Zhihui Liu, Heqiang Lou and Jiasheng Wu
J Integr Plant Biol 2023, 65 (8): 1904-1917.  
DOI: 10.1111/jipb.13501
Abstract (Browse 174)  |   Save
Plant growth and development are significantly hampered in saline environments, limiting agricultural productivity. Thus, it is crucial to unravel the mechanism underlying plant responses to salt stress. β-1,4-Galactan (galactan), which forms the side chains of pectic rhamnogalacturonan I, enhances plant sensitivity to high-salt stress. Galactan is synthesized by GALACTAN SYNTHASE1 (GALS1). We previously showed that NaCl relieves the direct suppression of GALS1 transcription by the transcription factors BPC1 and BPC2 to induce the excess accumulation of galactan in Arabidopsis (Arabidopsis thaliana). However, how plants adapt to this unfavorable environment remains unclear. Here, we determined that the transcription factors CBF1, CBF2, and CBF3 directly interact with the GALS1 promoter and repress its expression, leading to reduced galactan accumulation and enhanced salt tolerance. Salt stress enhances the binding of CBF1/CBF2/CBF3 to the GALS1 promoter by inducing CBF1/CBF2/CBF3 transcription and accumulation. Genetic analysis suggested that CBF1/CBF2/CBF3 function upstream of GALS1 to modulate salt-induced galactan biosynthesis and the salt response. CBF1/CBF2/CBF3 and BPC1/BPC2 function in parallel to regulate GALS1 expression, thereby modulating the salt response. Our results reveal a mechanism in which salt-activated CBF1/CBF2/CBF3 inhibit BPC1/BPC2-regulated GALS1 expression to alleviate galactan-induced salt hypersensitivity, providing an activation/deactivation fine-tune mechanism for dynamic regulation of GALS1 expression under salt stress in Arabidopsis.
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Cited: Web of Science(2)
Tyrosylprotein sulfotransferase suppresses ABA signaling via sulfation of SnRK2.2/2.3/2.6
Jun Wang, Chunyan Wang, Tianrun Wang, Shizhong Zhang, Kang Yan, Guodong Yang, Changai Wu, Chengchao Zheng and Jinguang Huang
J Integr Plant Biol 2023, 65 (8): 1846-1851.  
doi: 10.1111/jipb.13493
Abstract (Browse 170)  |   Save
Phytohormone abscisic acid (ABA) plays vital roles in stress tolerance, while long-term overactivation of ABA signaling suppresses plant growth and development. However, the braking mechanism of ABA responses is not clear. Protein tyrosine sulfation catalyzed by tyrosylprotein sulfotransferase (TPST) is a critical post-translational modification. Through genetic screening, we identified a tpst mutant in Arabidopsis that was hypersensitive to ABA. In-depth analysis revealed that TPST could interact with and sulfate SnRK2.2/2.3/2.6, which accelerated their degradation and weakened the ABA signaling. Taken together, these findings uncovered a novel mechanism of desensitizing ABA responses via protein sulfation.
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Rice pollen-specific OsRALF17 and OsRALF19 are essential for pollen tube growth
Eui‐Jung Kim, Ji‐Hyun Kim, Woo‐Jong Hong, Eun Young Kim, Myung‐Hee Kim, Su Kyoung Lee, Cheol Woo Min, Sun Tae Kim, Soon Ki Park, Ki‐Hong Jung and Yu‐Jin Kim
J Integr Plant Biol 2023, 65 (9): 2218-2236.  
doi: 10.1111/jipb.13508
Abstract (Browse 168)  |   Save
Pollen tube growth is essential for successful double fertilization, which is critical for grain yield in crop plants. Rapid alkalinization factors (RALFs) function as ligands for signal transduction during fertilization. However, functional studies on RALF in monocot plants are lacking. Herein, we functionally characterized two pollen-specific RALFs in rice (Oryza sativa) using multiple clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated protein 9-induced loss-of-function mutants, peptide treatment, expression analyses, and tag reporter lines. Among the 41 RALF members in rice, OsRALF17 was specifically expressed at the highest level in pollen and pollen tubes. Exogenously applied OsRALF17 or OsRALF19 peptide inhibited pollen tube germination and elongation at high concentrations but enhanced tube elongation at low concentrations, indicating growth regulation. Double mutants of OsRALF17 and OsRALF19 (ralf17/19) exhibited almost full male sterility with defects in pollen hydration, germination, and tube elongation, which was partially recovered by exogenous treatment with OsRALF17 peptide. This study revealed that two partially functionally redundant OsRALF17 and OsRALF19 bind to Oryza sativa male-gene transfer defective 2 (OsMTD2) and transmit reactive oxygen species signals for pollen tube germination and integrity maintenance in rice. Transcriptomic analysis confirmed their common downstream genes, in osmtd2 and ralf17/19. This study provides new insights into the role of RALF, expanding our knowledge of the biological role of RALF in regulating rice fertilization.
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CPR5 positively regulates pattern-triggered immunity via a mediator protein
Miaomiao Ma, Meng Li, Rongfang Zhou, Jian‐Bin Yu, Ying Wu, Xiaojuan Zhang, Jinlong Wang, Jian‐Min Zhou and Xiangxiu Liang
J Integr Plant Biol 2023, 65 (7): 1613-1619.  
doi: 10.1111/jipb.13472
Abstract (Browse 168)  |   Save
Plant cells possess a two-layered immune system consisting of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), mediated by cell surface pattern-recognition receptors and intracellular nucleotide-binding leucine-rich repeat receptors (NLRs), respectively. The CONSTITUTIVE EXPRESSION OF PR GENES 5 (CPR5) nuclear pore complex protein negatively regulates ETI, including ETI-associated hypersensitive response. Here, we show that CPR5 is essential for the activation of various PTI responses in Arabidopsis, such as resistance to the non-adapted bacterium Pseudomonas syringae pv. tomato DC3000 hrcC-. In a forward-genetic screen for suppressors of cpr5, we identified the mediator protein MED4. Mutation of MED4 in cpr5 greatly restored the defective PTI of cpr5. Our findings reveal that CPR5 plays opposite roles in regulating PTI and ETI, and genetically regulates PTI via MED4.
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Multi-omics analysis reveals the evolutionary origin of diterpenoid alkaloid biosynthesis pathways in Aconitum
Dake Zhao, Ya Zhang, Huanxing Ren, Yana Shi, Ding Dong, Zonghang Li, Guanghong Cui, Yong Shen, Zongmin Mou, Edward J. Kennelly, Luqi Huang, Jue Ruan, Suiyun Chen, Diqiu Yu and Yupeng Cun
J Integr Plant Biol 2023, 65 (10): 2320-2335.  
DOI: 10.1111/jipb.13565
Abstract (Browse 166)  |   Save
Diterpenoid alkaloids (DAs) have been often utilized in clinical practice due to their analgesic and anti-inflammatory properties. Natural DAs are prevalent in the family Ranunculaceae, notably in the Aconitum genus. Nevertheless, the evolutionary origin of the biosynthesis pathway responsible for DA production remains unknown. In this study, we successfully assembled a high-quality, pseudochromosome-level genome of the DA-rich species Aconitum vilmorinianum (A. vilmorinianum) (5.76 Gb). An A. vilmorinianum-specific whole-genome duplication event was discovered using comparative genomic analysis, which may aid in the evolution of the DA biosynthesis pathway. We identified several genes involved in DA biosynthesis via integrated genomic, transcriptomic, and metabolomic analyses. These genes included enzymes encoding target ent-kaurene oxidases and aminotransferases, which facilitated the activation of diterpenes and insertion of nitrogen atoms into diterpene skeletons, thereby mediating the transformation of diterpenes into DAs. The divergence periods of these genes in A. vilmorinianum were further assessed, and it was shown that two major types of genes were involved in the establishment of the DA biosynthesis pathway. Our integrated analysis offers fresh insights into the evolutionary origin of DAs in A. vilmorinianum as well as suggestions for engineering the biosynthetic pathways to obtain desired DAs.
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Elucidation of the melitidin biosynthesis pathway in pummelo
Shuangqian Shen, Shouchuang Wang, Chenkun Yang, Chao Wang, Qianqian Zhou, Shen Zhou, Ran Zhang, Yufei Li, Zixuan Wang, Liupan Dai, Wenjv Peng, Yingchen Hao, Hao Guo, Guangping Cao, Xianqing Liu, Fan Yao, Qiang Xu, Alisdair R. Fernie and Jie Luo
J Integr Plant Biol 2023, 65 (11): 2505-2518.  
DOI: 10.1111/jipb.13564
Abstract (Browse 165)  |   Save
Specialized plant metabolism is a rich resource of compounds for drug discovery. The acylated flavonoid glycoside melitidin is being developed as an anti-cholesterol statin drug candidate, but its biosynthetic route in plants has not yet been fully characterized. Here, we describe the gene discovery and functional characterization of a new flavonoid gene cluster (UDP-glucuronosyltransferases (CgUGTs), 1,2 rhamnosyltransferase (Cg1,2RhaT), acyltransferases (CgATs)) that is responsible for melitidin biosynthesis in pummelo (Citrus grandis (L.) Osbeck). Population variation analysis indicated that the tailoring of acyltransferases, specific for bitter substrates, mainly determine the natural abundance of melitidin. Moreover, 3-hydroxy-3-methylglutaryl-CoA reductase enzyme inhibition assays showed that the product from this metabolic gene cluster, melitidin, may be an effective anti-cholesterol statin drug candidate. Co-expression of these clustered genes in Nicotiana benthamiana resulted in the formation of melitidin, demonstrating the potential for metabolic engineering of melitidin in a heterologous plant system. This study establishes a biosynthetic pathway for melitidin, which provides genetic resources for the breeding and genetic improvement of pummelo aimed at fortifying the content of biologically active metabolites.
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Non-specific phospholipase C4 hydrolyzes phosphosphingolipids and phosphoglycerolipids and promotes rapeseed growth and yield
Bao Yang, Jianwu Li, Jiayu Yan, Ke Zhang, Zhewen Ouyang, Yefei Lu, Huili Wei, Qing Li, Xuan Yao, Shaoping Lu, Yueyun Hong, Xuemin Wang and Liang Guo
J Integr Plant Biol 2023, 65 (11): 2421-2436.  
DOI: 10.1111/jipb.13560
Abstract (Browse 165)  |   Save
Phosphorus is a major nutrient vital for plant growth and development, with a substantial amount of cellular phosphorus being used for the biosynthesis of membrane phospholipids. Here, we report that NON-SPECIFIC PHOSPHOLIPASE C4 (NPC4) in rapeseed (Brassica napus) releases phosphate from phospholipids to promote growth and seed yield, as plants with altered NPC4 levels showed significant changes in seed production under different phosphate conditions. Clustered regularly interspaced short palindromic repeat (CRISPR)/CRISPR-associated nuclease 9 (Cas9)-mediated knockout of BnaNPC4 led to elevated accumulation of phospholipids and decreased growth, whereas overexpression (OE) of BnaNPC4 resulted in lower phospholipid contents and increased plant growth and seed production. We demonstrate that BnaNPC4 hydrolyzes phosphosphingolipids and phosphoglycerolipids in vitro, and plants with altered BnaNPC4 function displayed changes in their sphingolipid and glycerolipid contents in roots, with a greater change in glycerolipids than sphingolipids in leaves, particularly under phosphate deficiency conditions. In addition, BnaNPC4-OE plants led to the upregulation of genes involved in lipid metabolism, phosphate release, and phosphate transport and an increase in free inorganic phosphate in leaves. These results indicate that BnaNPC4 hydrolyzes phosphosphingolipids and phosphoglycerolipids in rapeseed to enhance phosphate release from membrane phospholipids and promote growth and seed production.
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A loss-of-function mutant allele of a glycosyl hydrolase gene has been co-opted for seed weight control during soybean domestication
Siming Wei, Bin Yong, Hongwei Jiang, Zhenghong An, Yan Wang, Bingbing Li, Ce Yang, Weiwei Zhu, Qingshan Chen and Chaoying He
J Integr Plant Biol 2023, 65 (11): 2469-2489.  
DOI: 10.1111/jipb.13559
Abstract (Browse 164)  |   Save
The resultant DNA from loss-of-function mutation can be recruited in biological evolution and development. Here, we present such a rare and potential case of “to gain by loss” as a neomorphic mutation during soybean domestication for increasing seed weight. Using a population derived from a chromosome segment substitution line of Glycine max (SN14) and Glycine soja (ZYD06), a quantitative trait locus (QTL) of 100-seed weight (qHSW) was mapped on chromosome 11, corresponding to a truncated β-1, 3-glucosidase (βGlu) gene. The novel gene hsw results from a 14-bp deletion, causing a frameshift mutation and a premature stop codon in the βGlu. In contrast to HSW, the hsw completely lost βGlu activity and function but acquired a novel function to promote cell expansion, thus increasing seed weight. Overexpressing hsw instead of HSW produced large soybean seeds, and surprisingly, truncating hsw via gene editing further increased the seed size. We further found that the core 21-aa peptide of hsw and its variants acted as a promoter of seed size. Transcriptomic variation in these transgenic soybean lines substantiated the integration hsw into cell and seed size control. Moreover, the hsw allele underwent selection and expansion during soybean domestication and improvement. Our work cloned a likely domesticated QTL controlling soybean seed weight, revealed a novel genetic variation and mechanism in soybean domestication, and provided new insight into crop domestication and breeding, and plant evolution.
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Cited: Web of Science(2)
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