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    The OsAGO2–OsNAC300OsNAP module regulates leaf senescence in rice
    Shaoyan Zheng, Junyu Chen, Ying He, Jingqin Lu, Hong Chen, Zipeng Liang, Junqi Zhang, Zhenlan Liu, Jing Li, Chuxiong Zhuang
    J Integr Plant Biol 2024, 66 (11): 2395-2411.  
    doi: 10.1111/jipb.13766
    Abstract (Browse 78)  |   Save
    Leaves play a crucial role in the growth and development of rice (Oryza sativa) as sites for the production of photosynthesis. Early leaf senescence leads to substantial drops in rice yields. Whether and how DNA methylation regulates gene expression and affects leaf senescence remains elusive. Here, we demonstrate that mutations in rice ARGONAUTE 2 (OsAGO2) lead to premature leaf senescence, with chloroplasts in Osago2 having lower chlorophyll content and an abnormal thylakoid structure compared with those from wild-type plants. We show that OsAGO2 associates with a 24-nt microRNA and binds to the promoter region of OsNAC300, which causes DNA methylation and suppressed expression of OsNAC300. Overexpressing OsNAC300 causes the similar premature leaf senescence as Osago2 mutants and knocking out OsNAC300 in the Osago2 mutant background suppresses the early senescence of Osago2 mutants. Based on yeast one-hybrid, dual-luciferase, and electrophoresis mobility shift assays, we propose that OsNAC300 directly regulates transcription of the key rice aging gene NAC-like, activated by APETALA3/PISTILLATA (OsNAP) to control leaf senescence. Our results unravel a previously unknown epigenetic regulatory mechanism underlying leaf senescence in which OsAGO2–OsNAC300–OsNAP acts as a key regulatory module of leaf senescence to maintain leaf function.
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    AtVQ25 promotes salicylic acid-related leaf senescence by fine-tuning the self-repression of AtWRKY53
    Qi Tan, Mingming Zhao, Jingwei Gao, Ke Li, Mengwei Zhang, Yunjia Li, Zeting Liu, Yujia Song, Xiaoyue Lu, Zhengge Zhu, Rongcheng Lin, Pengcheng Yin, Chunjiang Zhou and Geng Wang
    J Integr Plant Biol 2024, 66 (6): 1126-1147.  
    DOI: 10.1111/jipb.13659
    Abstract (Browse 129)  |   Save
    Most mechanistic details of chronologically ordered regulation of leaf senescence are unknown. Regulatory networks centered on AtWRKY53 are crucial for orchestrating and integrating various senescence-related signals. Notably, AtWRKY53 binds to its own promoter and represses transcription of AtWRKY53, but the biological significance and mechanism underlying this self-repression remain unclear. In this study, we identified the VQ motif-containing protein AtVQ25 as a cooperator of AtWRKY53. The expression level of AtVQ25 peaked at mature stage and was specifically repressed after the onset of leaf senescence. AtVQ25-overexpressing plants and atvq25 mutants displayed precocious and delayed leaf senescence, respectively. Importantly, we identified AtWRKY53 as an interacting partner of AtVQ25. We determined that interaction between AtVQ25 and AtWRKY53 prevented AtWRKY53 from binding to W-box elements on the AtWRKY53 promoter and thus counteracted the self-repression of AtWRKY53. In addition, our RNA-sequencing data revealed that the AtVQ25-AtWRKY53 module is related to the salicylic acid (SA) pathway. Precocious leaf senescence and SA-induced leaf senescence in AtVQ25-overexpressing lines were inhibited by an SA pathway mutant, atsid2, and NahG transgenic plants; AtVQ25-overexpressing/atwrky53 plants were also insensitive to SA-induced leaf senescence. Collectively, we demonstrated that AtVQ25 directly attenuates the self-repression of AtWRKY53 during the onset of leaf senescence, which is substantially helpful for understanding the timing of leaf senescence onset modulated by AtWRKY53.
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    Functional divergences of natural variations of TaNAM-A1 in controlling leaf senescence during wheat grain filling
    Longxi Zhou, Guowei Chang, Chuncai Shen, Wan Teng, Xue He, Xueqiang Zhao, Yanfu Jing, Zhixiong Huang and Yiping Tong
    J Integr Plant Biol 2024, 66 (6): 1242-1260.  
    DOI: 10.1111/jipb.13658
    Abstract (Browse 121)  |   Save
    Leaf senescence is an essential physiological process related to grain yield potential and nutritional quality. Green leaf duration (GLD) after anthesis directly reflects the leaf senescence process and exhibits large genotypic differences in common wheat; however, the underlying gene regulatory mechanism is still lacking. Here, we identified TaNAM-A1 as the causal gene of the major loci qGLD-6A for GLD during grain filling by map-based cloning. Transgenic assays and TILLING mutant analyses demonstrated that TaNAM-A1 played a critical role in regulating leaf senescence, and also affected spike length and grain size. Furthermore, the functional divergences among the three haplotypes of TaNAM-A1 were systematically evaluated. Wheat varieties with TaNAM-A1d (containing two mutations in the coding DNA sequence of TaNAM-A1) exhibited a longer GLD and superior yield-related traits compared to those with the wild type TaNAM-A1a. All three haplotypes were functional in activating the expression of genes involved in macromolecule degradation and mineral nutrient remobilization, with TaNAM-A1a showing the strongest activity and TaNAM-A1d the weakest. TaNAM-A1 also modulated the expression of the senescence-related transcription factors TaNAC-S-7A and TaNAC016-3A. TaNAC016-3A enhanced the transcriptional activation ability of TaNAM-A1a by protein-protein interaction, thereby promoting the senescence process. Our study offers new insights into the fine-tuning of the leaf functional period and grain yield formation for wheat breeding under various geographical climatic conditions.
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    ERF5 enhances protocorm-like body regeneration via enhancement of STM expression in Dendrobium orchid
    Danqi Zeng, Can Si, Mingze Zhang, Jun Duan and Chunmei He
    J Integr Plant Biol 2023, 65 (9): 2071-2085.  
    DOI: 10.1111/jipb.13534
    Abstract (Browse 174)  |   Save
    Orchid plants develop protocorms upon germination and produce protocorm-like structures called protocorm-like bodies (PLBs) from protocorms and somatic cells via tissue culture. Protocorm-like bodies have broad technical application potential in the orchid industry and their regeneration is a distinct developmental process in the plant kingdom. However, little is known about this unparalleled developmental program. In this study, we identified a PLB-abundant gene, ethylene response factor (ERF), and a transcription factor named DoERF5, and determined its important role in PLB regeneration in Dendrobium orchid. Overexpression of DoERF5 in Dendrobium greatly enhanced the PLB regeneration from PLB and stem explants, and upregulated the expression of WOUND-INDUCED DEDIFFERENTIATION (DoWIND) homologs and SHOOT MERISTEMLESS (DoSTM), as well as the genes involved in cytokinin biosynthesis (DoIPT) and the cytokinin response factors (DoARRs). However, silencing DoERF5 reduced the regeneration rate of PLBs, and downregulated the expression of DoWIND homologs, DoSTM and DoARRs. We demonstrated that DoERF5 is directly bound to the DoSTM promoter and regulates its expression. In addition, overexpression of DoSTM in Dendrobium orchid resulted in favorable regeneration of PLBs. Our results clarify that DoERF5 regulates the regeneration of PLB by enhancing DoSTM expression. Our findings provide new insights into how DoERF5 mediates PLB regeneration and offers technical potential in improving clonal propagation, preservation, and the bioengineering of orchids.
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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 223)  |   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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    Regulation of FLC nuclear import by coordinated action of the NUP62-subcomplex and importin β SAD2
    Gang Chen, Danyun Xu, Qing Liu, Zhichuang Yue, Biao Dai, Shujuan Pan, Yongqiang Chen, Xinhua Feng and Honghong Hu
    J Integr Plant Biol 2023, 65 (9): 2086-2106.  
    DOI: 10.1111/jipb.13540
    Abstract (Browse 197)  |   Save
    Flowering locus C (FLC) is a central transcriptional repressor that controls flowering time. However, how FLC is imported into the nucleus is unknown. Here, we report that Arabidopsis nucleoporins 62 (NUP62), NUP58, and NUP54 composed NUP62-subcomplex modulates FLC nuclear import during floral transition in an importin α-independent manner, via direct interaction. NUP62 recruits FLC to the cytoplasmic filaments and imports it into the nucleus through the NUP62-subcomplex composed central channel. Importin β supersensitive to ABA and drought 2 (SAD2), a carrier protein, is critical for FLC nuclear import and flower transition, which facilitates FLC import into the nucleus mainly through the NUP62-subcomplex. Proteomics, RNA-seq, and cell biological analyses indicate that the NUP62-subcomplex mainly mediates the nuclear import of cargos with unconventional nuclear localization sequences (NLSs), such as FLC. Our findings illustrate the mechanisms of the NUP62-subcomplex and SAD2 on FLC nuclear import process and floral transition, and provide insights into the role of NUP62-subcomplex and SAD2 in protein nucleocytoplasmic transport in plants.
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    FIGL1 coordinates with dosage-sensitive BRCA2 in modulating meiotic recombination in maize
    Ting Zhang, Shuang‐Hui Zhao, Yan Wang and Yan He
    J Integr Plant Biol 2023, 65 (9): 2107-2121.  
    DOI: 10.1111/jipb.13541
    Abstract (Browse 182)  |   Save
    Meiotic crossover (CO) formation between homologous chromosomes ensures their subsequent proper segregation and generates genetic diversity among offspring. In maize, however, the mechanisms that modulate CO formation remain poorly characterized. Here, we found that both maize BREAST CANCER SUSCEPTIBILITY PROTEIN 2 (BRCA2) and AAA-ATPase FIDGETIN-LIKE-1 (FIGL1) act as positive factors of CO formation by controlling the assembly or/and stability of two conserved DNA recombinases RAD51 and DMC1 filaments. Our results revealed that ZmBRCA2 is not only involved in the repair of DNA double-stranded breaks (DSBs), but also regulates CO formation in a dosage-dependent manner. In addition, ZmFIGL1 interacts with RAD51 and DMC1, and Zmfigl1 mutants had a significantly reduced number of RAD51/DMC1 foci and COs. Further, simultaneous loss of ZmFIGL1 and ZmBRCA2 abolished RAD51/DMC1 foci and exacerbated meiotic defects compared with the single mutant Zmbrca2 or Zmfigl1. Together, our data demonstrate that ZmBRCA2 and ZmFIGL1 act coordinately to regulate the dynamics of RAD51/DMC1-dependent DSB repair to promote CO formation in maize. This conclusion is surprisingly different from the antagonistic roles of BRCA2 and FIGL1 in Arabidopsis, implying that, although key factors that control CO formation are evolutionarily conserved, specific characteristics have been adopted in diverse plant species.
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    α-Ketoglutarate dehydrogenase (KGDH): A new balancer between energy metabolism and gene expression in plants
    Wenwen Zhu and Yikun He
    J Integr Plant Biol 2023, 65 (8): 1843-1845.  
    doi: 10.1111/jipb.13544
    Abstract (Browse 152)  |   Save
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    Scaffold protein RACK1A positively regulates leaf senescence by coordinating the EIN3-miR164-ORE1 transcriptional cascade in Arabidopsis
    Jan Masood, Wei Zhu, Yajuan Fu, Zhiyong Li, Yeling Zhou, Dong Zhang, Huihui Han, Yan Yan, Xing Wen, Hongwei Guo and Jiansheng Liang
    J Integr Plant Biol 2023, 65 (7): 1703-1716.  
    DOI: 10.1111/jipb.13483
    Abstract (Browse 208)  |   Save
    Plants have adopted versatile scaffold proteins to facilitate the crosstalk between multiple signaling pathways. Leaf senescence is a well-programmed developmental stage that is coordinated by various external and internal signals. However, the functions of plant scaffold proteins in response to senescence signals are not well understood. Here, we report that the scaffold protein RACK1A (RECEPTOR FOR ACTIVATED C KINASE 1A) participates in leaf senescence mediated by ethylene signaling via the coordination of the EIN3-miR164-ORE1 transcriptional regulatory cascade. RACK1A is a novel positive regulator of ethylene-mediated leaf senescence. The rack1a mutant exhibits delayed leaf senescence, while transgenic lines overexpressing RACK1A display early leaf senescence. Moreover, RACK1A promotes EIN3 (ETHYLENE INSENSITIVE 3) protein accumulation, and directly interacts with EIN3 to enhance its DNA-binding activity. Together, they then associate with the miR164 promoter to inhibit its transcription, leading to the release of the inhibition on downstream ORE1 (ORESARA 1) transcription and the promotion of leaf senescence. This study reveals a mechanistic framework by which RACK1A promotes leaf senescence via the EIN3-miR164-ORE1 transcriptional cascade, and provides a paradigm for how scaffold proteins finely tune phytohormone signaling to control plant development.
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    Cited: Web of Science(1)
      
    ESCRT-III component OsSNF7.2 modulates leaf rolling by trafficking and endosomal degradation of auxin biosynthetic enzyme OsYUC8 in rice
    Liang Zhou, Saihua Chen, Maohong Cai, Song Cui, Yulong Ren, Xinyue Zhang, Tianzhen Liu, Chunlei Zhou, Xin Jin, Limin Zhang, Minxi Wu, Shuyi Zhang, Zhijun Cheng, Xin Zhang, Cailin Lei, Qibing Lin, Xiuping Guo, Jie Wang, Zhichao Zhao, Ling Jiang, Shanshan Zhu and Jianmin Wan
    J Integr Plant Biol 2023, 65 (6): 1408-1422.  
    DOI: 10.1111/jipb.13460
    Abstract (Browse 317)  |   Save
    The endosomal sorting complex required for transport (ESCRT) is highly conserved in eukaryotic cells and plays an essential role in the biogenesis of multivesicular bodies and cargo degradation to the plant vacuole or lysosomes. Although ESCRT components affect a variety of plant growth and development processes, their impact on leaf development is rarely reported. Here, we found that OsSNF7.2, an ESCRT-III component, controls leaf rolling in rice (Oryza sativa). The Ossnf7.2 mutant rolled leaf 17 (rl17) has adaxially rolled leaves due to the decreased number and size of the bulliform cells. OsSNF7.2 is expressed ubiquitously in all tissues, and its protein is localized in the endosomal compartments. OsSNF7.2 homologs, including OsSNF7, OsSNF7.3, and OsSNF7.4, can physically interact with OsSNF7.2, but their single mutation did not result in leaf rolling. Other ESCRT complex subunits, namely OsVPS20, OsVPS24, and OsBRO1, also interact with OsSNF7.2. Further assays revealed that OsSNF7.2 interacts with OsYUC8 and aids its vacuolar degradation. Both Osyuc8 and rl17 Osyuc8 showed rolled leaves, indicating that OsYUC8 and OsSNF7.2 function in the same pathway, conferring leaf development. This study reveals a new biological function for the ESCRT-III components, and provides new insights into the molecular mechanisms underlying leaf rolling.
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    Cited: Web of Science(4)
      
    Transcription factor GLK1 promotes anthocyanin biosynthesis via an MBW complex-dependent pathway in Arabidopsis thaliana
    Yan Li, Wei Lei, Zuxu Zhou, Yanlin Li, Dawei Zhang and Honghui Lin
    J Integr Plant Biol 2023, 65 (6): 1521-1535.  
    DOI: 10.1111/jipb.13471
    Abstract (Browse 296)  |   Save
    Anthocyanins are important natural plant pigments and play diverse roles in plant growth and adaptation. Anthocyanins function as screens to protect photosynthetic tissues from photoinhibition. However, the regulatory mechanisms underlying the biosynthesis and spatial accumulation pattern of anthocyanins remain some unresolved issues. Here, we demonstrate that the GARP-type transcription factor GOLDEN2-LIKE 1 (GLK1) functions as a positive factor in anthocyanin accumulation. GLK1 enhances the transcriptional activation activities of MYB75, MYB90, and MYB113 via direct protein- protein interactions to increase the expression of anthocyanin-specific biosynthetic genes. Anthocyanins accumulate in an acropetal manner in Arabidopsis. We also found that the expression pattern of GLK1 overall mimicked the accumulation pattern of anthocyanin from the base of the main stem to the shoot apex. Based on these findings, we established a working model for the role of GLK1 in anthocyanin accumulation and propose that GLK1 mediates the spatial distribution pattern of anthocyanins by affecting the transcriptional activation activities of MYB75, MYB90, and MYB113.
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    Cited: Web of Science(2)
      
    Translation rate underpins specific targeting of N-terminal transmembrane proteins to mitochondria
    Junho Lee, Byeongho Moon, Dong Wook Lee and Inhwan Hwang
    J Integr Plant Biol 2023, 65 (6): 1505-1520.  
    DOI: 10.1111/jipb.13475
    Abstract (Browse 141)  |   Save
    Protein biogenesis is a complex process, and complexity is greatly increased in eukaryotic cells through specific targeting of proteins to different organelles. To direct targeting, organellar proteins carry an organelle-specific targeting signal for recognition by organelle-specific import machinery. However, the situation is confusing for transmembrane domain (TMD)-containing signal- anchored (SA) proteins of various organelles because TMDs function as an endoplasmic reticulum (ER) targeting signal. Although ER targeting of SA proteins is well understood, how they are targeted to mitochondria and chloroplasts remains elusive. Here, we investigated how the targeting specificity of SA proteins is determined for specific targeting to mitochondria and chloroplasts. Mitochondrial targeting requires multiple motifs around and within TMDs: a basic residue and an arginine-rich region flanking the N- and C-termini of TMDs, respectively, and an aromatic residue in the C-terminal side of the TMD that specify mitochondrial targeting in an additive manner. These motifs play a role in slowing down the elongation speed during translation, thereby ensuring mitochondrial targeting in a co- translational manner. By contrast, the absence of any of these motifs individually or together causes at varying degrees chloroplast targeting that occurs in a post-translational manner.
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    Cited: Web of Science(1)
      
    Reciprocal inhibition of expression between RAV1 and BES1 modulates plant growth and development in Arabidopsis
    Dami Yang, Hyun‐young Shin, Hyun Kyung Kang, Yun Shang, So Young Park, Dong‐Hoon Jeong and Kyoung Hee Nam
    J Integr Plant Biol 2023, 65 (5): 1226-1240.  
    doi: 10.1111/jipb.13431
    Abstract (Browse 139)  |   Save
    RAV1 (Related to ABI3/VP1) is a plant‐specific B3 and AP2 domain‐containing transcription factor that acts as a negative regulator of growth in many plant species. The expression of RAV1 is downregulated by brassinosteroids (BRs); large‐scale transcriptome analyses have shown that the expression of RAV1 was previously targeted by BRI1‐EMS‐SUPPRESOR1 (BES1) and BRASSINAZOLE‐RESISTANT1 (BZR1), which are critical transcription factors for the BR‐ signaling process. Using RAV1‐overexpressing transgenic plants, we showed that RAV1 overexpression reduced the BR signaling capacity, resulting in the downregulation of BR biosynthetic genes and BES1 expression. Furthermore, we demonstrated that BES1, not BZR1, is directly bound to the RAV1 promoter and repressed RAV1 expression, and vice versa; RAV1 is also bound to the BES1 promoter and repressed BES1 expression. This mutual inhibition was specific to RAV1 and BES1 because RAV1 exhibited binding activity to the BZR1 promoter but did not repress BZR1 expression. We observed that constitutively activated BR signaling phenotypes in bes1‐D were attenuated by the repression of endogenous BES1 expression in transgenic bes1‐D plants overexpressing RAV1. RNA‐ sequencing analysis of RAV1‐overexpressing transgenic plants and bes1‐D mutant plants revealed differentially expressed genes by RAV1 and BES1 and genes that were oppositely co‐regulated by RAV1 and BES1. RAV1 and BES1 regulated different transcriptomes but co‐regulated a specific set of genes responsible for the balance between growth and defense. These results suggested that the mutual inhibitory transcriptional activities of RAV1 and BES1 provide fine regulatory mechanisms for plant growth and development.
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    PagERF81 regulates lignin biosynthesis and xylem cell differentiation in poplar
    Xin‐Wei Zhao, Qiao Wang, Dian Wang, Wei Guo, Meng‐Xuan Hu, Ying‐Li Liu, Gong‐Ke Zhou, Guo‐Hua Chai, Shu‐Tang Zhao and Meng‐Zhu Lu
    J Integr Plant Biol 2023, 65 (5): 1134-1146.  
    DOI: 10.1111/jipb.13453
    Abstract (Browse 304)  |   Save
    Lignin is a major component of plant cell walls and is essential for plant growth and development. Lignin biosynthesis is controlled by a hierarchical regulatory network involving multiple transcription factors. In this study, we showed that the gene encoding an APETALA 2/ethylene-responsive element binding factor (AP2/ERF) transcription factor, PagERF81, from poplar 84?K (Populus alba × P. glandulosa) is highly expressed in expanding secondary xylem cells. Two independent homozygous Pagerf81 mutant lines created by gene editing, produced significantly more but smaller vessel cells and longer fiber cells with more lignin in cell walls, while PagERF81 overexpression lines had less lignin, compared to non-transgenic controls. Transcriptome and reverse transcription quantitative PCR data revealed that multiple lignin biosynthesis genes including Cinnamoyl CoA reductase 1 (PagCCR1), Cinnamyl alcohol dehydrogenase 6 (PagCAD6), and 4-Coumarate-CoA ligase-like 9 (Pag4CLL9) were up-regulated in Pagerf81 mutants, but down-regulated in PagERF81 overexpression lines. In addition, a transient transactivation assay revealed that PagERF81 repressed the transcription of these three genes. Furthermore, yeast one hybrid and electrophoretic mobility shift assays showed that PagERF81 directly bound to a GCC sequence in the PagCCR1 promoter. No known vessel or fiber cell differentiation related genes were differentially expressed, so the smaller vessel cells and longer fiber cells observed in the Pagerf81 lines might be caused by abnormal lignin deposition in the secondary cell walls. This study provides insight into the regulation of lignin biosynthesis, and a molecular tool to engineer wood with high lignin content, which would contribute to the lignin-related chemical industry and carbon sequestration.
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    Cited: Web of Science(1)
      
    ANAC087 transcription factor positively regulates age-dependent leaf senescence through modulating the expression of multiple target genes in Arabidopsis
    Qinqin Chen, Jingli Yan, Tiantian Tong, Peiyu Zhao, Shuangshuang Wang, Na Zhou, Xing Cui, Moyu Dai, Yuan‐Qing Jiang and Bo Yang
    J Integr Plant Biol 2023, 65 (4): 967-984.  
    DOI: 10.1111/jipb.13434
    Abstract (Browse 352)  |   Save
    Leaf senescence is the final stage of leaf development and appropriate onset and progression of leaf senescence are critical for reproductive success and fitness. Although great progress has been made in identifying key genes regulating leaf senescence and elucidating the underlining mechanisms in the model plant Arabidopsis, there is still a gap to understanding the complex regulatory network. In this study, we discovered that Arabidopsis ANAC087 transcription factor (TF) positively modulated leaf senescence. Expression of ANAC087 was induced in senescing leaves and the encoded protein acted as a transcriptional activator. Both constitutive and inducible overexpression lines of ANAC087 showed earlier senescence than control plants, whereas T‐DNA insertion mutation and dominant repression of the ANAC087 delayed senescence rate. A quantitative reverse transcription‐polymerase chain reaction (qRT‐ PCR) profiling showed that the expression of an array of senescence‐associated genes was upregulated in inducible ANAC087 overexpression plants including BFN1, NYE1, CEP1, RbohD, SAG13, SAG15, and VPEs, which are involved in programmed cell death (PCD), chlorophyll degradation and reactive oxygen species (ROS) accumulation. In addition, electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation‐quantitative polymerase chain reaction (ChIP‐qPCR) assays demonstrated that ANAC087 directly bound to the canonical NAC recognition sequence (NACRS) motif in promoters of its target genes. Moreover, mutation of two representative target genes, BFN1 or NYE1 alleviated the senescence rate of ANAC087‐overexpression plants, suggesting their genetic regulatory relationship. Taken together, this study indicates that ANAC087 serves as an important regulator linking PCD, ROS, and chlorophyll degradation to leaf senescence.
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    Cited: Web of Science(2)
      
    IQ67 DOMAIN protein 21 is critical for indentation formation in pavement cell morphogenesis
    Xinhua Feng, Shujuan Pan, Haifu Tu, Junjie Huang, Chuanlei Xiao, Xin Shen, Lei You, Xinyan Zhao, Yongqiang Chen, Danyun Xu, Xiaolu Qu and Honghong Hu
    J Integr Plant Biol 2023, 65 (3): 721-738.  
    DOI: 10.1111/jipb.13393
    Abstract (Browse 195)  |   Save
    In plants, cortical microtubules anchor to the plasma membrane in arrays and play important roles in cell shape. However, the molecular mechanism of microtubule binding proteins, which connect the plasma membrane and cortical microtubules in cell morphology remains largely unknown. Here, we report that a plasma membrane and microtubule dual-localized IQ67 domain protein, IQD21, is critical for cotyledon pavement cell (PC) morphogenesis in Arabidopsis. iqd21 mutation caused increased indentation width, decreased lobe length, and similar lobe number of PCs, whereas IQD21 overexpression had a different effect on cotyledon PC shape. Weak overexpression led to increased lobe number, decreased indentation width, and similar lobe length, while moderate or great overexpression resulted in decreased lobe number, indentation width, and lobe length of PCs. Live-cell observations revealed that IQD21 accumulation at indentation regions correlates with lobe initiation and outgrowth during PC development. Cell biological and genetic approaches revealed that IQD21 promotes transfacial microtubules anchoring to the plasma membrane via its polybasic sites and bundling at the indentation regions in both periclinal and anticlinal walls. IQD21 controls cortical microtubule organization mainly through promoting Katanin 1-mediated microtubule severing during PC interdigitation. These findings provide the genetic evidence that transfacial microtubule arrays play a determinant role in lobe formation, and the insight into the molecular mechanism of IQD21 in transfacial microtubule organization at indentations and puzzle-shaped PC development.
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    Cited: Web of Science(7)
      
    Advances in structure and function of auxin response factor in plants
    Yonghui Li, Shaqila Han and Yanhua Qi
    J Integr Plant Biol 2023, 65 (3): 617-632.  
    DOI: 10.1111/jipb.13392
    Abstract (Browse 284)  |   Save
    Auxin is a crucial phytohormone that has various effects on the regulators of plant growth and development. Auxin signal transduction is mainly controlled by two gene families: auxin response factor (ARF) and auxin/indole-3-acetic acid (Aux/IAA). ARFs are plant-specific transcription factors that bind directly to auxin response elements in the promoters of auxin-responsive genes. ARF proteins contain three conserved regions: a conserved N-terminal B3 DNA-binding domain, a variable intermediate middle region domain that functions in activation or repression, and a C-terminal domain including the Phox and Bem1p region for dimerization, similar to the III and IV elements of Aux/IAA, which facilitate protein–protein interaction through homodimerization of ARF proteins or heterodimerization of ARF and Aux/IAA proteins. In the two decades following the identification of the first ARF, 23 ARF members have been identified and characterized in Arabidopsis. Using whole-genome sequencing, 22, 25, 23, 25, and 36 ARF genes have been identified in tomato, rice, wheat, sorghum, and maize, respectively, in addition to which the related biofunctions of some ARFs have been reported. ARFs play crucial roles in regulating the growth and development of roots, leaves, flowers, fruits, seeds, responses to biotic and abiotic stresses, and phytohormone signal crosstalk. In this review, we summarize the research progress on the structures and functions of ARFs in Arabidopsis, tomato, and cereal crops, to provide clues for future basic research on phytohormone signaling and the molecular design breeding of crops.
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    Cited: Web of Science(15)
      
    Low copy numbers for mitochondrial DNA moderates the strength of nuclear–cytoplasmic incompatibility in plants
    Liguang Zhang, Jin Ma, Zhaorui Shen, Bo Wang, Qingling Jiang, Fei Ma, Yan Ju, Guangxing Duan, Quan Zhang, Xiaodong Su and Sodmergen
    J Integr Plant Biol 2023, 65 (3): 739-754.  
    DOI: 10.1111/jipb.13400
    Abstract (Browse 190)  |   Save
    Plant cells contain only small amounts of mitochondrial DNA (mtDNA), with the genomic information shared among multiple mitochondria. The biological relevance and molecular mechanism underlying this hallmark of plant cells has been unclear. Here, we report that Arabidopsis thaliana plants exhibited significantly reduced growth and mitochondrial dysfunction when the mtDNA copy number was increased to the degree that each mitochondrion possessed DNA. The amounts of mitochondrion-encoded transcripts increased several fold in the presence of elevated mtDNA levels. However, the efficiency of RNA editing decreased with this excess of mitochondrion-encoded transcripts, resulting in impaired assembly of mitochondrial complexes containing mtDNA-encoded subunits, such as respiratory complexes I and IV. These observations indicate the occurrence of nuclear–mitochondrial incompatibility in the cells with increased amounts of mtDNA and provide an initial answer to the fundamental question of why plant cells have much lower mtDNA levels than animal cells. We propose that keeping mtDNA levels low moderates nuclear–mitochondrial incompatibility and that this may be a crucial factor driving plant cells to restrict the copy numbers of mtDNA.
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    Coronatine promotes maize water uptake by directly binding to the aquaporin ZmPIP2;5 and enhancing its activity
    Rui He, Huiqing Su, Xing Wang, Zhijie Ren, Kun Zhang, Tianyu Feng, Mingcai Zhang, Zhaohu Li, Legong Li, Junhong Zhuang, Zhizhong Gong, Yuyi Zhou and Liusheng Duan
    J Integr Plant Biol 2023, 65 (3): 703-720.  
    DOI: 10.1111/jipb.13432
    Abstract (Browse 148)  |   Save
    Water uptake is crucial for crop growth and development and drought stress tolerance. The water channel aquaporins (AQP) play important roles in plant water uptake. Here, we discovered that a jasmonic acid analog, coronatine (COR), enhanced maize (Zea mays) root water uptake capacity under artificial water deficiency conditions. COR treatment induced the expression of the AQP gene Plasma membrane intrinsic protein 2;5 (ZmPIP2;5). In vivo and in vitro experiments indicated that COR also directly acts on ZmPIP2;5 to improve water uptake in maize and Xenopus oocytes. The leaf water potential and hydraulic conductivity of roots growing under hyperosmotic conditions were higher in ZmPIP2;5-overexpression lines and lower in the zmpip2;5 knockout mutant, compared to wild-type plants. Based on a comparison between ZmPIP2;5 and other PIP2s, we predicted that COR may bind to the functional site in loop E of ZmPIP2;5. We confirmed this prediction by surface plasmon resonance technology and a microscale thermophoresis assay, and showed that deleting the binding motif greatly reduced COR binding. We identified the N241 residue as the COR-specific binding site, which may activate the channel of the AQP tetramer and increase water transport activity, which may facilitate water uptake under hyperosmotic stress.
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    Understanding protein translocation across chloroplast membranes: Translocons and motor proteins
    Da Been Kim, Changhee Na, Inhwan Hwang and Dong Wook Lee
    J Integr Plant Biol 2023, 65 (2): 408-416.  
    doi: 10.1111/jipb.13385
    Abstract (Browse 184)  |   Save
    Subcellular organelles in eukaryotes are surrounded by lipid membranes. In an endomembrane system, vesicle trafficking is the primary mechanism for the delivery of organellar proteins to specific organelles. However, organellar proteins for chloroplasts, mitochondria, the nucleus, and peroxisomes that are translated in the cytosol are directly imported into their target organelles. Chloroplasts are a plant-specific organelle with outer and inner envelope membranes, a dual-membrane structure that is similar to mitochondria. Interior chloroplast proteins translated by cytosolic ribosomes are thus translocated through TOC and TIC complexes (translocons in the outer and inner envelope of chloroplasts, respectively), with stromal ATPase motor proteins playing a critical role in pulling pre-proteins through these import channels. Over the last three decades, the identity and function of TOC/TIC components and stromal motor proteins have been actively investigated, which has shed light on the action mechanisms at a molecular level. However, there remains some disagreement over the exact composition of TIC complexes and genuine stromal motor proteins. In this review, we discuss recent findings on the mechanisms by which proteins are translocated through TOC/TIC complexes and discuss future prospects for this field of research.
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    To curve for survival: Apical hook development
    Yichuan Wang, Yang Peng and Hongwei Guo
    J Integr Plant Biol 2023, 65 (2): 324-342.  
    doi: 10.1111/jipb.13441
    Abstract (Browse 186)  |   Save
    Apical hook is a simple curved structure formed at the upper part of hypocotyls when dicot seeds germinate in darkness. The hook structure is transient but essential for seedlings' survival during soil emergence due to its efficient protection of the delicate shoot apex from mechanical injury. As a superb model system for studying plant differential growth, apical hook has fascinated botanists as early as the Darwin age, and significant advances have been achieved at both the morphological and molecular levels to understand how apical hook development is regulated. Here, we will mainly summarize the research progress at these two levels. We will also briefly compare the growth dynamics between apical hook and hypocotyl gravitropic bending at early seed germination phase, with the aim to deduce a certain consensus on their connections. Finally, we will outline the remaining questions and future research perspectives for apical hook development.
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    Cited: Web of Science(3)
      
    Asymmetric cell division in plant development
    Yi Zhang, Tongda Xu and Juan Dong
    J Integr Plant Biol 2023, 65 (2): 343-370.  
    doi: 10.1111/jipb.13446
    Abstract (Browse 211)  |   Save
    Asymmetric cell division (ACD) is a fundamental process that generates new cell types during development in eukaryotic species. In plant development, post-embryonic organogenesis driven by ACD is universal and more important than in animals, in which organ pattern is preset during embryogenesis. Thus, plant development provides a powerful system to study molecular mechanisms underlying ACD. During the past decade, tremendous progress has been made in our understanding of the key components and mechanisms involved in this important process in plants. Here, we present an overview of how ACD is determined and regulated in multiple biological processes in plant development and compare their conservation and specificity among different model cell systems. We also summarize the molecular roles and mechanisms of the phytohormones in the regulation of plant ACD. Finally, we conclude with the overarching paradigms and principles that govern plant ACD and consider how new technologies can be exploited to fill the knowledge gaps and make new advances in the field.
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    Cited: Web of Science(2)
      
    ARK2 stabilizes the plus-end of microtubules and promotes microtubule bundling in Arabidopsis
    Miao Lan, Xianan Liu, Erfang Kang, Ying Fu, Lei Zhu
    J Integr Plant Biol 2023, 65 (1): 100-116.  
    DOI: 10.1111/jipb.13373
    Abstract (Browse 170)  |   Save
    Microtubule dynamics and organization are important for plant cell morphogenesis and development. The microtubule-based motor protein kinesins are mainly responsible for the transport of some organelles and vesicles, although several have also been shown to regulate microtubule organization. The ARMADILLO REPEAT KINESIN (ARK) family is a plant-specific motor protein subfamily that consists of three members (ARK1, ARK2, and ARK3) in Arabidopsis thaliana. ARK2 has been shown to participate in root epidermal cell morphogenesis. However, whether and how ARK2 associates with microtubules needs further elucidation. Here, we demonstrated that ARK2 co-localizes with microtubules and facilitates microtubule bundling in vitro and in vivo. Pharmacological assays and microtubule dynamics analyses indicated that ARK2 stabilizes cortical microtubules. Live-cell imaging revealed that ARK2 moves along cortical microtubules in a processive mode and localizes both at the plus-end and the sidewall of microtubules. ARK2 therefore tracks and stabilizes the growing plus-ends of microtubules, which facilitates the formation of parallel microtubule bundles.
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    Cited: Web of Science(1)
      
    OpNAC1 transcription factor regulates the biosynthesis of the anticancer drug camptothecin by targeting loganic acid O-methyltransferase in Ophiorrhiza pumila
    Xiaolong Hao, Can Wang, Wei Zhou, Qingyan Ruan, Chenhong Xie, Yinkai Yang, Chengyu Xiao, Yan Cai, Jingyi Wang, Yao Wang, Xuebin Zhang, Itay Maoz, Guoyin Kai
    J Integr Plant Biol 2023, 65 (1): 133-149.  
    DOI: 10.1111/jipb.13377
    Abstract (Browse 275)  |   Save
    Camptothecin (CPT) is an anticancer pentacyclic quinoline alkaloid widely used to treat cancer patients worldwide. However, the biosynthetic pathway and transcriptional regulation of camptothecin are largely unknown. Ophiorrhiza pumila, the herbaceous plant from the Rubiaceae family, has emerged as a model plant for studying camptothecin biosynthesis and regulation. In this study, a high-quality reference genome of O. pumila with estimated size of ~456.90?Mb was reported, and the accumulation level of camptothecin in roots was higher than that in stems and leaves. Based on its spatial distribution in the plant, we examined gene functions and expression by combining genomics with transcriptomic analysis. Two loganic acid O-methyltransferase (OpLAMTs) were identified in strictosidine-producing plant O. pumila, and enzyme catalysis assays showed that OpLAMT1 and not OpLAMT2 could convert loganic acid into loganin. Further knock-out of OpLAMT1 expression led to the elimination of loganin and camptothecin accumulation in O. pumila hairy roots. Four key residues were identified in OpLAMT1 protein crucial for the catalytic activity of loganic acid to loganin. By co-expression network, we identified a NAC transcription factor, OpNAC1, as a candidate gene for regulating camptothecin biosynthesis. Transgenic hairy roots and biochemical assays demonstrated that OpNAC1 suppressed OpLAMT1 expression. Here, we reported on two camptothecin metabolic engineering strategies paving the road for industrial-scale production of camptothecin in CPT-producing plants.
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    Cited: Web of Science(2)
      
    Response to Zhang et al., ‘do egg cell-secreted aspartic proteases promote gamete attachment?’
    Jiahao Jiang, Li-Jia Qu
    J Integr Plant Biol 2023, 65 (1): 7-9.  
    doi: 10.1111/jipb.13448
    Abstract (Browse 178)  |   Save
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    Cited: Web of Science(1)
      
    Do egg cell-secreted aspartic proteases promote gamete attachment?
    Xuecheng Zhang, Xiaobo Yu, Ce Shi, Thomas Dresselhaus, Meng-Xiang Sun
    J Integr Plant Biol 2023, 65 (1): 3-6.  
    doi: 10.1111/jipb.13447
    Abstract (Browse 154)  |   Save
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    Cited: Web of Science(1)
      
    R-loop: The new genome regulatory element in plants
    Jincong Zhou, Weifeng Zhang, Qianwen Sun
    J Integr Plant Biol 2022, 64 (12): 2275-2289.  
    doi: 10.1111/jipb.13383
    Abstract (Browse 219)  |   Save

    An R-loop is a three-stranded chromatin structure that consists of a displaced single strand of DNA and an RNA:DNA hybrid duplex, which was thought to be a rare by-product of transcription. However, recent genome-wide data have shown that R-loops are widespread and pervasive in a variety of genomes, and a growing body of experimental evidence indicates that R-loops have both beneficial and harmful effects on an organism. To maximize benefit and avoid harm, organisms have evolved several means by which they tightly regulate R-loop levels. Here, we summarize our current understanding of the biogenesis and effects of R-loops, the mechanisms that regulate them, and methods of R-loop profiling, reviewing recent research advances on R-loops in plants. Furthermore, we provide perspectives on future research directions for R-loop biology in plants, which might lead to a more comprehensive understanding of R-loop functions in plant genome regulation and contribute to future agricultural improvements.

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    Cited: Web of Science(4)
      
    High auxin stimulates callus through SDG8-mediated histone H3K36 methylation in Arabidopsis
    Jun Ma, Qiang Li, Lei Zhang, Sen Cai, Yuanyuan Liu, Juncheng Lin, Rongfeng Huang, Yongqiang Yu, Mingzhang Wen and Tongda Xu
    J Integr Plant Biol 2022, 64 (12): 2425-2437.  
    doi: 10.1111/jipb.13387
    Abstract (Browse 172)  |   Save

    Callus induction, which results in fate transition in plant cells, is considered as the first and key step for plant regeneration. This process can be stimulated in different tissues by a callus-inducing medium (CIM), which contains a high concentration of phytohormone auxin. Although a few key regulators for callus induction have been identified, the multiple aspects of the regulatory mechanism driven by high levels of auxin still need further investigation. Here, we find that high auxin induces callus through a H3K36 histone methylation-dependent mechanism, which requires the methyltransferase SET DOMAIN GROUP 8 (SDG8). During callus induction, the increased auxin accumulates SDG8 expression through a TIR1/AFBs-based transcriptional regulation. SDG8 then deposits H3K36me3 modifications on the loci of callus-related genes, including a master regulator WOX5 and the cell proliferation-related genes, such as CYCB1.1. This epigenetic regulation in turn is required for the transcriptional activation of these genes during callus formation. These findings suggest that the massive transcriptional reprogramming for cell fate transition by auxin during callus formation requires epigenetic modifications including SDG8-mediated histone H3K36 methylation. Our results provide insight into the coordination between auxin signaling and epigenetic regulation during fundamental processes in plant development.

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    Arabidopsis Trithorax histone methyltransferases are redundant in regulating development and DNA methylation
    Ji-Yun Shang, Xue-Wei Cai, Yin-Na Su, Zhao-Chen Zhang, Xin Wang, Nan Zhao and Xin-Jian He
    J Integr Plant Biol 2022, 64 (12): 2438-2454.  
    doi: 10.1111/jipb.13406
    Abstract (Browse 215)  |   Save

    Although the Trithorax histone methyltransferases ATX1–5 are known to regulate development and stress responses by catalyzing histone H3K4 methylation in Arabidopsis thaliana, it is unknown whether and how these histone methyltransferases affect DNA methylation. Here, we found that the redundant ATX1–5 proteins are not only required for plant development and viability but also for the regulation of DNA methylation. The expression and H3K4me3 levels of both RNA-directed DNA methylation (RdDM) genes (NRPE1, DCL3, IDN2, and IDP2) and active DNA demethylation genes (ROS1, DML2, and DML3) were downregulated in the atx1/2/4/5 mutant. Consistent with the facts that the active DNA demethylation pathway mediates DNA demethylation mainly at CG and CHG sites, and that the RdDM pathway mediates DNA methylation mainly at CHH sites, whole-genome DNA methylation analyses showed that hyper-CG and CHG DMRs in atx1/2/4/5 significantly overlapped with those in the DNA demethylation pathway mutant ros1 dml2 dml3 (rdd), and that hypo-CHH DMRs in atx1/2/4/5 significantly overlapped with those in the RdDM mutant nrpe1, suggesting that the ATX paralogues function redundantly to regulate DNA methylation by promoting H3K4me3 levels and expression levels of both RdDM genes and active DNA demethylation genes. Given that the ATX proteins function as catalytic subunits of COMPASS histone methyltransferase complexes, we also demonstrated that the COMPASS complex components function as a whole to regulate DNA methylation. This study reveals a previously uncharacterized mechanism underlying the regulation of DNA methylation.

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    Cited: Web of Science(1)
      
    Active DNA demethylation in plants: 20 years of discovery and beyond
    Heng Zhang, Zhizhong Gong and Jian-Kang Zhu
    J Integr Plant Biol 2022, 64 (12): 2217-2239.  
    doi: 10.1111/jipb.13423
    Abstract (Browse 204)  |   Save

    Maintaining proper DNA methylation levels in the genome requires active demethylation of DNA. However, removing the methyl group from a modified cytosine is chemically difficult and therefore, the underlying mechanism of demethylation had remained unclear for many years. The discovery of the first eukaryotic DNA demethylase, Arabidopsis thaliana REPRESSOR OF SILENCING 1 (ROS1), led to elucidation of the 5-methylcytosine base excision repair mechanism of active DNA demethylation. In the 20 years since ROS1 was discovered, our understanding of this active DNA demethylation pathway, as well as its regulation and biological functions in plants, has greatly expanded. These exciting developments have laid the groundwork for further dissecting the regulatory mechanisms of active DNA demethylation, with potential applications in epigenome editing to facilitate crop breeding and gene therapy.

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    Cited: Web of Science(2)
      
    The plant circadian clock regulates autophagy rhythm through transcription factor LUX ARRHYTHMO
    Ming‐Kang Yang, Xiao‐Jie Zhu, Chu‐Min Chen, Xu Guo, Shu‐Xuan Xu, Ya‐Rou Xu, Shen‐Xiu Du, Shi Xiao, Bernd Mueller‐Roeber, Wei Huang and Liang Chen
    J Integr Plant Biol 2022, 64 (11): 2135-2149.  
    doi: 10.1111/jipb.13343
    Abstract (Browse 189)  |   Save

    Autophagy is an evolutionarily conserved degradation pathway in eukaryotes; it plays a critical role in nutritional stress tolerance. The circadian clock is an endogenous timekeeping system that generates biological rhythms to adapt to daily changes in the environment. Accumulating evidence indicates that the circadian clock and autophagy are intimately interwoven in animals. However, the role of the circadian clock in regulating autophagy has been poorly elucidated in plants. Here, we show that autophagy exhibits a robust circadian rhythm in both light/dark cycle (LD) and in constant light (LL) in Arabidopsis. However, autophagy rhythm showed a different pattern with a phase-advance shift and a lower amplitude in LL compared to LD. Moreover, mutation of the transcription factor LUX ARRHYTHMO (LUX) removed autophagy rhythm in LL and led to an enhanced amplitude in LD. LUX represses expression of the core autophagy genes ATG2, ATG8a, and ATG11 by directly binding to their promoters. Phenotypic analysis revealed that LUX is responsible for improved resistance of plants to carbon starvation, which is dependent on moderate autophagy activity. Comprehensive transcriptomic analysis revealed that the autophagy rhythm is ubiquitous in plants. Taken together, our findings demonstrate that the LUX-mediated circadian clock regulates plant autophagy rhythms.

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    Cited: Web of Science(5)
      
    The transcriptional co-repressor SEED DORMANCY 4-LIKE (AtSDR4L) promotes the embryonic-to-vegetative transition in Arabidopsis thaliana
    Ting Wu, Milad Alizadeh, Bailan Lu, Jinkui Cheng, Ryan Hoy, Miaoyu Bu, Emma Laqua, Dongxue Tang, Junna He, Dongeun Go, Zhizhong Gong and Liang Song
    J Integr Plant Biol 2022, 64 (11): 2075-2096.  
    DOI: 10.1111/jipb.13360
    Abstract (Browse 198)  |   Save

    Repression of embryonic traits during the seed-to-seedling phase transition requires the inactivation of master transcription factors associated with embryogenesis. How the timing of such inactivation is controlled is unclear. Here, we report on a novel transcriptional co-repressor, Arabidopsis thaliana SDR4L, that forms a feedback inhibition loop with the master transcription factors LEC1 and ABI3 to repress embryonic traits post-imbibition. LEC1 and ABI3 regulate their own expression by inducing AtSDR4L during mid to late embryogenesis. AtSDR4L binds to sites upstream of LEC1 and ABI4, and these transcripts are upregulated in Atsdr4l seedlings. Atsdr4l seedlings phenocopy a LEC1 overexpressor. The embryonic traits of Atsdr4l can be partially rescued by impairing LEC1 or ABI3. The penetrance and expressivity of the Atsdr4l phenotypes depend on both developmental and external cues, demonstrating the importance of AtSDR4L in seedling establishment under suboptimal conditions.

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    Cited: Web of Science(3)
      
    The egg cell is preferentially fertilized in Arabidopsis double fertilization
    Ling Li, Saiying Hou, Wei Xiang, Zihan Song, Yuan Wang, Li Zhang, Jing Li, Hongya Gu, Juan Dong, Thomas Dresselhaus, Sheng Zhong and Li-Jia Qu
    J Integr Plant Biol 2022, 64 (11): 2039-2046.  
    doi: 10.1111/jipb.13370
    Abstract (Browse 246)  |   Save
    Each cyclin-dependent kinase a;1 mutant pollen grain contains a single sperm-like cell that can fertilize egg cells, similar to sperm cells. Pollination assays with mutant pollen demonstrated that the egg cell is preferentially fertilized in Arabidopsis.
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    Egg cell-secreted aspartic proteases ECS1/2 promote gamete attachment to prioritize the fertilization of egg cells over central cells in Arabidopsis
    Jiahao Jiang, Nils Stührwohldt, Tianxu Liu, Qingpei Huang, Ling Li, Li Zhang, Hongya Gu, Liumin Fan, Sheng Zhong, Andreas Schaller and Li-Jia Qu
    J Integr Plant Biol 2022, 64 (11): 2047-2059.  
    DOI: 10.1111/jipb.13371
    Abstract (Browse 256)  |   Save

    Double fertilization is an innovative phenomenon in angiosperms, in which one sperm cell first fuses with the egg cell to produce the embryo, and then the other sperm fuses with the central cell to produce the endosperm. However, the molecular mechanism of the preferential fertilization of egg cells is poorly understood. In this study, we report that two egg cell-secreted aspartic proteases, ECS1 and ECS2, play an important role in promoting preferential fertilization of egg cells in Arabidopsis. We show that simultaneous loss of ECS1 and ECS2 function resulted in an approximately 20% reduction in fertility, which can be complemented by the full-length ECS1/2 but not by corresponding active site mutants or by secretion-defective versions of ECS1/2. Detailed phenotypic analysis revealed that the egg cell–sperm cell attachment was compromised in ecs1 ecs2 siliques. Limited pollination assays with cyclin-dependent kinase a1 (cdka;1) pollen showed that preferential egg cell fertilization was impaired in the ecs1 ecs2 mutant. Taken together, these results demonstrate that egg cells secret two aspartic proteases, ECS1 and ECS2, to facilitate the attachment of sperm cells to egg cells so that preferential fertilization of egg cells is achieved. This study reveals the molecular mechanism of preferential fertilization in Arabidopsis thaliana.

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    Arabidopsis mitochondrial single-stranded DNA-binding proteins SSB1 and SSB2 are essential regulators of mtDNA replication and homologous recombination
    Jie Qian, Min Zheng, Lingyu Wang, Yu Song, Jiawen Yan and Yi‐Feng Hsu
    J Integr Plant Biol 2022, 64 (10): 1952-1965.  
    DOI: 10.1111/jipb.13338
    Abstract (Browse 159)  |   Save
    Faithful DNA replication is one of the most essential processes in almost all living organisms. However, the proteins responsible for organellar DNA replication are still largely unknown in plants. Here, we show that the two mitochondrion-targeted single-stranded DNA-binding (SSB) proteins SSB1 and SSB2 directly interact with each other and act as key factors for mitochondrial DNA (mtDNA) maintenance, as their single or double loss-of-function mutants exhibit severe germination delay and growth retardation. The mtDNA levels in mutants lacking SSB1 and/or SSB2 function were two- to four-fold higher than in the wild-type (WT), revealing a negative role for SSB1/2 in regulating mtDNA replication. Genetic analysis indicated that SSB1 functions upstream of mitochondrial DNA POLYMERASE IA (POLIA) or POLIB in mtDNA replication, as mutation in either gene restored the high mtDNA copy number of the ssb1-1 mutant back to WT levels. In addition, SSB1 and SSB2 also participate in mitochondrial genome maintenance by influencing mtDNA homologous recombination (HR). Additional genetic analysis suggested that SSB1 functions upstream of ORGANELLAR SINGLE-STRANDED DNA-BINDING PROTEIN1 (OSB1) during mtDNA replication, while SSB1 may act downstream of OSB1 and MUTS HOMOLOG1 for mtDNA HR. Overall, our results yield new insights into the roles of the plant mitochondrion-targeted SSB proteins and OSB1 in maintaining mtDNA stability via affecting DNA replication and DNA HR.
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    Cited: Web of Science(2)
      
    The unconventional prefoldin RPB5 interactor mediates the gravitropic response by modulating cytoskeleton organization and auxin transport in Arabidopsis
    Yi Yang, Fang Liu, Le Liu, Mingyue Zhu, Jinfeng Yuan, Yan‐Xia Mai, Jun‐Jie Zou, Jie Le, Yonghong Wang, Klaus Palme, Xugang Li, Yong Wang and Long Wang
    J Integr Plant Biol 2022, 64 (10): 1916-1934.  
    doi: 10.1111/jipb.13341
    Abstract (Browse 184)  |   Save
    Gravity-induced root curvature involves the asymmetric distribution of the phytohormone auxin. This response depends on the concerted activities of the auxin transporters such as PIN-FORMED (PIN) proteins for auxin efflux and AUXIN RESISTANT 1 (AUX1) for auxin influx. However, how the auxin gradient is established remains elusive. Here we identified a new mutant with a short root, strong auxin distribution in the lateral root cap and an impaired gravitropic response. The causal gene encoded an Arabidopsis homolog of the human unconventional prefoldin RPB5 interactor (URI). AtURI interacted with prefoldin 2 (PFD2) and PFD6, two β-type PFD members that modulate actin and tubulin patterning in roots. The auxin reporter DR5rev:GFP showed that asymmetric auxin redistribution after gravistimulation is disordered in aturi-1 root tips. Treatment with the endomembrane protein trafficking inhibitor brefeldin A indicated that recycling of the auxin transporter PIN2 is disrupted in aturi-1 roots as well as in pfd mutants. We propose that AtURI cooperates with PFDs to recycle PIN2 and modulate auxin distribution.
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    Engineering of triterpene metabolism and overexpression of the lignin biosynthesis gene PAL promotes ginsenoside Rg3 accumulation in ginseng plant chassis
    Lu Yao, Huanyu Zhang, Yirong Liu, Qiushuang Ji, Jing Xie, Ru Zhang, Luqi Huang, Kunrong Mei, Juan Wang and Wenyuan Gao
    J Integr Plant Biol 2022, 64 (9): 1739-1754.  
    DOI: 10.1111/jipb.13315
    Abstract (Browse 275)  |   Save

    The ginsenoside Rg3 found in Panax species has extensive pharmacological properties, in particular anti-cancer effects. However, its natural yield in Panax plants is limited. Here, we report a multi-modular strategy to improve yields of Rg3 in a Panax ginseng chassis, combining engineering of triterpene metabolism and overexpression of a lignin biosynthesis gene, phenylalanine ammonia lyase (PAL). We first performed semi-rational design and site mutagenesis to improve the enzymatic efficiency of Pq3-O-UGT2, a glycosyltransferase that directly catalyzes the biosynthesis of Rg3 from Rh2. Next, we used clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) gene editing to knock down the branch pathway of protopanaxatriol-type ginsenoside biosynthesis to enhance the metabolic flux of the protopanaxadiol-type ginsenoside Rg3. Overexpression of PAL accelerated the formation of the xylem structure, significantly improving ginsenoside Rg3 accumulation (to 6.19-fold higher than in the control). We combined overexpression of the ginsenoside aglycon synthetic genes squalene epoxidase, Pq3-O-UGT2, and PAL with CRISPR/Cas9-based knockdown of CYP716A53v2 to improve ginsenoside Rg3 accumulation. Finally, we produced ginsenoside Rg3 at a yield of 83.6 mg/L in a shake flask (7.0 mg/g dry weight, 21.12-fold higher than with wild-type cultures). The high-production system established in this study could be a potential platform to produce the ginsenoside Rg3 commercially for pharmaceutical use.

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    ERF4 interacts with and antagonizes TCP15 in regulating endoreduplication and cell growth in Arabidopsis
    An‐Ming Ding, Chuan‐Tao Xu, Qiang Xie, Ming‐Jin Zhang, Ning Yan, Chang‐Bo Dai, Jing Lv, Meng‐Meng Cui, Wei‐Feng Wang and Yu‐He Sun
    J Integr Plant Biol 2022, 64 (9): 1673-1689.  
    DOI: 10.1111/jipb.13323
    Abstract (Browse 276)  |   Save

    Endoreduplication is prevalent during plant growth and development, and is often correlated with large cell and organ size. Despite its prevalence, the transcriptional regulatory mechanisms underlying the transition from mitotic cell division to endoreduplication remain elusive. Here, we characterize ETHYLENE-RESPONSIVE ELEMENT BINDING FACTOR 4 (ERF4) as a positive regulator of endoreduplication through its function as a transcriptional repressor. ERF4 was specifically expressed in mature tissues in which the cells were undergoing expansion, but was rarely expressed in young organs. Plants overexpressing ERF4 exhibited much larger cells and organs, while plants that lacked functional ERF4 displayed smaller organs than the wild-type. ERF4 was further shown to regulate cell size by controlling the endopolyploidy level in the nuclei. Moreover, ERF4 physically associates with the class I TEOSINTE BRANCHED 1/CYCLOIDEA/PCF (TCP) protein TCP15, a transcription factor that inhibits endoreduplication by activating the expression of a key cell-cycle gene, CYCLIN A2;3 (CYCA2;3). A molecular and genetic analysis revealed that ERF4 promotes endoreduplication by directly suppressing the expression of CYCA2;3. Together, this study demonstrates that ERF4 and TCP15 function as a module to antagonistically regulate each other's activity in regulating downstream genes, thereby controlling the switch from the mitotic cell cycle to endoreduplication during leaf development. These findings expand our understanding of how the control of the cell cycle is fine-tuned by an ERF4–TCP15 transcriptional complex.

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    PP2A interacts with KATANIN to promote microtubule organization and conical cell morphogenesis
    Huibo Ren, Jinqiu Rao, Min Tang, Yaxing Li, Xie Dang and Deshu Lin
    J Integr Plant Biol 2022, 64 (8): 1514-1530.  
    DOI: 10.1111/jipb.13281
    Abstract (Browse 1251)  |   Save

    The organization of the microtubule cytoskeleton is critical for cell and organ morphogenesis. The evolutionarily conserved microtubule-severing enzyme KATANIN plays critical roles in microtubule organization in the plant and animal kingdoms. We previously used conical cell of Arabidopsis thaliana petals as a model system to investigate cortical microtubule organization and cell morphogenesis and determined that KATANIN promotes the formation of circumferential cortical microtubule arrays in conical cells. Here, we demonstrate that the conserved protein phosphatase PP2A interacts with and dephosphorylates KATANIN to promote the formation of circumferential cortical microtubule arrays in conical cells. KATANIN undergoes cycles of phosphorylation and dephosphorylation. Using co-immunoprecipitation coupled with mass spectrometry, we identified PP2A subunits as KATANIN-interacting proteins. Further biochemical studies showed that PP2A interacts with and dephosphorylates KATANIN to stabilize its cellular abundance. Similar to the katanin mutant, mutants for genes encoding PP2A subunits showed disordered cortical microtubule arrays and defective conical cell shape. Taken together, these findings identify PP2A as a regulator of conical cell shape and suggest that PP2A mediates KATANIN phospho-regulation during plant cell morphogenesis.

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    Vitamin B1 THIAMIN REQUIRING1 synthase mediates the maintenance of chloroplast function by regulating sugar and fatty acid metabolism in rice
    Yanshen Nie, Li Yu, Lianlian Mao, Wenxuan Zou, Xiufeng Zhang and Jie Zhao
    J Integr Plant Biol 2022, 64 (8): 1575-1595.  
    DOI: 10.1111/jipb.13283
    Abstract (Browse 357)  |   Save

    Vitamin B1 (VB1), including thiamin, thiamin monophosphate (TMP), and thiamin pyrophosphate (TPP), is an essential micronutrient for all living organisms. Nevertheless, the precise function of VB1 in rice remains unclear. Here, we described a VB1 auxotrophic mutant, chlorotic lethal seedling (cles) from the mutation of OsTH1, which displayed collapsed chloroplast membrane system and decreased pigment content. OsTH1 encoded a phosphomethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase, and was expressed in various tissues, especially in seedlings, leaves, and young panicles. The VB1 content in cles was markedly reduced, despite an increase in the expression of VB1 synthesis genes. The decreased TPP content affected the tricarboxylic acid cycle, pentose phosphate pathway, and de novo fatty acid synthesis, leading to a reduction in fatty acids (C16:0 and C18:0) and sugars (sucrose and glucose) of cles. Additionally, irregular expression of chloroplast membrane synthesis genes led to membrane collapse. We also found that alternative splicing and translation allowed OsTH1 to be localized to both chloroplast and cytosol. Our study revealed that OsTH1 was an essential enzyme in VB1 biosynthesis and played crucial roles in seedling growth and development by participating in fatty acid and sugar metabolism, providing new perspectives on VB1 function in rice.

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    Cited: Web of Science(1)
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