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    Phase separation in plants: New insights into cellular compartmentalization
    Xiumei Xu, Canhui Zheng, Dandan Lu, Chun‐Peng Song and Lixin Zhang
    J Integr Plant Biol 2021, 63 (11): 1835-1855.  
    doi: 10.1111/jipb.13152
    Abstract (Browse 350)  |   Save
    A fundamental challenge for cells is how to coordinate various biochemical reactions in space and time. To achieve spatiotemporal control, cells have developed organelles that are surrounded by lipid bilayer membranes. Further, membraneless compartmentalization, a process induced by dynamic physical association of biomolecules through phase transition offers another efficient mechanism for intracellular organization. While our understanding of phase separation was predominantly dependent on yeast and animal models, recent findings have provided compelling evidence for emerging roles of phase separation in plants. In this review, we first provide an overview of the current knowledge of phase separation, including its definition, biophysical principles, molecular features and regulatory mechanisms. Then we summarize plant-specific phase separation phenomena and describe their functions in plant biological processes in great detail. Moreover, we propose that phase separation is an evolutionarily conserved and efficient mechanism for cellular compartmentalization which allows for distinct metabolic processes and signaling pathways, and is especially beneficial for the sessile lifestyle of plants to quickly and efficiently respond to the changing environment.
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    PagGRF12a interacts with PagGIF1b to regulate secondary xylem development through modulating PagXND1a expression in Populus alba × P. glandulosa
    Jinnan Wang, Houjun Zhou, Yanqiu Zhao, Cheng Jiang, Jihong Li, Fang Tang, Yingli Liu, Shutang Zhao, Jianjun Hu, Xueqin Song and Meng‐Zhu Lu
    J Integr Plant Biol 2021, 63 (10): 1683-1694.  
    DOI: 10.1111/jipb.13102
    Abstract (Browse 253)  |   Save
    Growth-regulating factors (GRFs) are important regulators of plant development and growth, but their possible roles in xylem development in woody plants remain unclear. Here, we report that Populus alba × Papulus glandulosa PagGRF12a negatively regulates xylem development in poplar. PagGRF12a is expressed in vascular tissues. Compared to non-transgenic control plants, transgenic poplar plants overexpressing PagGRF12a exhibited reduced xylem width and plants with repressed expression of PagGRF12a exhibited increased xylem width. Xylem NAC domain 1 (XND1) encodes a NAC domain transcription factor that regulates xylem development and transcriptional analyses revealed that PagXND1a is highly upregulated in PagGRF12a-overexpressing plants and downregulated in PagGRF12a-suppressed plants, indicating that PagGRF12a may regulate xylem development through PagXND1a. Transient transcriptional assays and chromatin immunoprecipitation-polymerase chain reaction assays confirmed that PagGRF12a directly upregulates PagXND1a. In addition, PagGRF12a interacts with the GRF-Interacting Factor (GIF) PagGIF1b, and this interaction enhances the effects of PagGRF12a on PagXND1a. Our results indicate that PagGRF12a inhibits xylem development by upregulating the expression of PagXND1a.
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    CDE4 encodes a pentatricopeptide repeat protein involved in chloroplast RNA splicing and affects chloroplast development under low-temperature conditions in rice
    Xinyong Liu, Xichun Zhang, Ruijie Cao, Guiai Jiao, Shikai Hu, Gaoneng Shao, Zhonghua Sheng, Lihong Xie, Shaoqing Tang, Xiangjin Wei and Peisong Hu
    J Integr Plant Biol 2021, 63 (10): 1724-1739.  
    doi: 10.1111/jipb.13147
    Abstract (Browse 292)  |   Save
    Pentatricopeptide repeat (PPR) proteins play important roles in the post-transcriptional modification of organellar RNAs in plants. However, the function of most PPR proteins remains unknown. Here, we characterized the rice (Oryza sativa L.) chlorophyll deficient 4 (cde4) mutant which exhibits an albino phenotype during early leaf development, with decreased chlorophyll contents and abnormal chloroplasts at low-temperature (20°C). Positional cloning revealed that CDE4 encodes a P-type PPR protein localized in chloroplasts. In the cde4 mutant, plastid-encoded polymerase (PEP)-dependent transcript levels were significantly reduced, but transcript levels of nuclear-encoded genes were increased compared to wild-type plants at 20°C. CDE4 directly binds to the transcripts of the chloroplast genes rpl2, ndhA, and ndhB. Intron splicing of these transcripts was defective in the cde4 mutant at 20°C, but was normal at 32°C. Moreover, CDE4 interacts with the guanylate kinase VIRESCENT 2 (V2); overexpression of V2 enhanced CDE4 protein stability, thereby rescuing the cde4 phenotype at 20°C. Our results suggest that CDE4 participates in plastid RNA splicing and plays an important role in rice chloroplast development under low-temperature conditions.
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    The rice Raf-like MAPKKK OsILA1 confers broad-spectrum resistance to bacterial blight by suppressing the OsMAPKK4–OsMAPK6 cascade
    Jie Chen, Lihan Wang, Zeyu Yang, Hongbo Liu, Chuanliang Chu, Zhenzhen Zhang, Qinglu Zhang, Xianghua Li, Jinghua Xiao, Shiping Wang and Meng Yuan
    J Integr Plant Biol 2021, 63 (10): 1815-1832.  
    DOI: 10.1111/jipb.13150
    Abstract (Browse 290)  |   Save
    Mitogen-activated protein kinase kinase kinase (MAPKKK) are the first components of MAPK cascades, which play pivotal roles in signaling during plant development and physiological processes. The genome of rice encodes 75 MAPKKKs, of which 43 are Raf-like MAPKKKs. The functions and action modes of most of the Raf-like MAPKKKs, whether they function as bona fide MAPKKKs and which are their downstream MAPKKs, are largely unknown. Here, we identified the osmapkkk43 mutant, which conferred broad-spectrum resistance to Xanthomonas oryzae pv. oryzae (Xoo), the destructive bacterial pathogen of rice. Oryza sativa (Os)MAPKKK43 encoding a Raf-like MAPKKK was previously known as Increased Leaf Angle 1 (OsILA1). Genetic analysis indicated that OsILA1 functioned as a negative regulator and acted upstream of the OsMAPKK4–OsMAPK6 cascade in rice–Xoo interactions. Unlike classical MAPKKKs, OsILA1 mainly phosphorylated the threonine 34 site at the N-terminal domain of OsMAPKK4, which possibly influenced the stability of OsMAPKK4. The N-terminal domain of OsILA1 is required for its homodimer formation and its full phosphorylation capacity. Taken together, our findings reveal that OsILA1 acts as a negative regulator of the OsMAPKK4–OsMAPK6 cascade and is involved in rice–Xoo interactions.
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    Engineering broad-spectrum disease-resistant rice by editing multiple susceptibility genes
    Hui Tao, Xuetao Shi, Feng He, Dan Wang, Ning Xiao, Hong Fang, Ruyi Wang, Fan Zhang, Min Wang, Aihong Li, Xionglun Liu, Guo‐Liang Wang and Yuese Ning
    J Integr Plant Biol 2021, 63 (9): 1639-1648.  
    doi: 10.1111/jipb.13145
    Abstract (Browse 311)  |   Save
    Rice blast and bacterial blight are important diseases of rice (Oryza sativa) caused by the fungus Magnaporthe oryzae and the bacterium Xanthomonas oryzae pv. oryzae (Xoo), respectively. Breeding rice varieties for broad-spectrum resistance is considered the most effective and sustainable approach to controlling both diseases. Although dominant resistance genes have been extensively used in rice breeding and production, generating disease-resistant varieties by altering susceptibility (S) genes that facilitate pathogen compatibility remains unexplored. Here, using CRISPR/Cas9 technology, we generated loss-of-function mutants of the S genes Pi21 and Bsr-d1 and showed that they had increased resistance to M. oryzae. We also generated a knockout mutant of the S gene Xa5 that showed increased resistance to Xoo. Remarkably, a triple mutant of all three S genes had significantly enhanced resistance to both M. oryzae and Xoo. Moreover, the triple mutant was comparable to the wild type in regard to key agronomic traits, including plant height, effective panicle number per plant, grain number per panicle, seed setting rate, and thousand-grain weight. These results demonstrate that the simultaneous editing of multiple S genes is a powerful strategy for generating new rice varieties with broad-spectrum resistance.
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    LjaFGD: Lonicera japonica functional genomics database
    Qiaoqiao Xiao, Zhongqiu Li, Mengmeng Qu, Wenying Xu, Zhen Su and Jiaotong Yang
    J Integr Plant Biol 2021, 63 (8): 1422-1436.  
    DOI: 10.1111/jipb.13112
    Abstract (Browse 222)  |   Save
    Lonicera japonica Thunb., a traditional Chinese herb, has been used for treating human diseases for thousands of years. Recently, the genome of L. japonica has been decoded, providing valuable information for research into gene function. However, no comprehensive database for gene functional analysis and mining is available for L. japonica. We therefore constructed LjaFGD (www.gzybioinformatics.cn/LjaFGD and bioinformatics.cau.edu.cn/LjaFGD), a database for analyzing and comparing gene function in L. japonica. We constructed a gene co-expression network based on 77 RNA-seq samples, and then annotated genes of L. japonica by alignment against protein sequences from public databases. We also introduced several tools for gene functional analysis, including Blast, motif analysis, gene set enrichment analysis, heatmap analysis, and JBrowse. Our co-expression network revealed that MYB and WRKY transcription factor family genes were co-expressed with genes encoding key enzymes in the biosynthesis of chlorogenic acid and luteolin in L. japonica. We used flavonol synthase 1 (LjFLS1) as an example to show the reliability and applicability of our database. LjaFGD and its various associated tools will provide researchers with an accessible platform for retrieving functional information on L. japonica genes to further biological discovery.
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    Circadian rhythms driving a fast-paced root clock implicate species-specific regulation in Medicago truncatula
    Liping Wang, Anqi Zhou, Jing Li, Mingkang Yang, Fan Bu, Liangfa Ge, Liang Chen and Wei Huang
    J Integr Plant Biol 2021, 63 (8): 1537-1554.  
    doi: 10.1111/jipb.13138
    Abstract (Browse 261)  |   Save
    Plants have a hierarchical circadian structure comprising multiple tissue-specific oscillators that operate at different speeds and regulate the expression of distinct sets of genes in different organs. However, the identity of the genes differentially regulated by the circadian clock in different organs, such as roots, and how their oscillations create functional specialization remain unclear. Here, we profiled the diurnal and circadian landscapes of the shoots and roots of Medicago truncatula and identified the conserved regulatory sequences contributing to transcriptome oscillations in each organ. We found that the light-dark cycles strongly affect the global transcriptome oscillation in roots, and many clock genes oscillate only in shoots. Moreover, many key genes involved in nitrogen fixation are regulated by circadian rhythms. Surprisingly, the root clock runs faster than the shoot clock, which is contrary to the hierarchical circadian structure showing a slow-paced root clock in both detached and intact Arabidopsis thaliana (L.) Heynh. roots. Our result provides important clues about the species-specific circadian regulatory mechanism, which is often overlooked, and possibly coordinates the timing between shoots and roots independent of the current prevailing model.
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    Rice SPL10 positively regulates trichome development through expression of HL6 and auxin-related genes
    Jinjie Li, Bo Tang, Yingxiu Li, Chenguang Li, Minjie Guo, Haiyang Chen, Shichen Han, Jin Li, Qijin Lou, Wenqiang Sun, Peng Wang, Haifeng Guo, Wei Ye, Zhanying Zhang, Hongliang Zhang, Sibin Yu, Long Zhang and Zichao Li
    J Integr Plant Biol 2021, 63 (8): 1521-1537.  
    DOI: 10.1111/jipb.13140
    Abstract (Browse 382)  |   Save
    Trichomes function in plant defenses against biotic and abiotic stresses; examination of glabrous lines, which lack trichomes, has revealed key aspects of trichome development and function. Tests of allelism in 51 glabrous rice (Oryza sativa) accessions collected worldwide identified OsSPL10 and OsWOX3B as regulators of trichome development in rice. Here, we report that OsSPL10 acts as a transcriptional regulator controlling trichome development. Haplotype and transient expression analyses revealed that variation in the approximately 700-bp OsSPL10 promoter region is the primary cause of the glabrous phenotype in the indica cultivar WD-17993. Disruption of OsSPL10 by genome editing decreased leaf trichome density and length in the NIL-HL6 background. Plants with genotype OsSPL10WD-17993/HL6 generated by crossing WD-17993 with NIL-HL6 also had fewer trichomes in the glumes. HAIRY LEAF6 (HL6) encodes another transcription factor that regulates trichome initiation and elongation, and OsSPL10 directly binds to the HL6 promoter to regulate its expression. Moreover, the transcript levels of auxin-related genes, such as OsYUCCA5 and OsPIN-FORMED1b, were altered in OsSPL10 overexpression and RNAi transgenic lines. Feeding tests using locusts (Locusta migratoria) demonstrated that non-glandular trichomes affect feeding by this herbivore. Our findings provide a molecular framework for trichome development and an ecological perspective on trichome functions.
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    Primary root and root hair development regulation by OsAUX4 and its participation in the phosphate starvation response
    Rigui Ye, Yunrong Wu, Zhenyu Gao, Hao Chen, Lixia Jia, Dongming Li, Xugang Li, Qian Qian and Yanhua Qi
    J Integr Plant Biol 2021, 63 (8): 1555-1567.  
    DOI: 10.1111/jipb.13142
    Abstract (Browse 255)  |   Save
    Among the five members of AUX1/LAX genes coding for auxin carriers in rice, only OsAUX1 and OsAUX3 have been reported. To understand the function of the other AUX1/LAX genes, two independent alleles of osaux4 mutants, osaux4-1 and osaux4-2, were constructed using the CRISPR/Cas9 editing system. Homozygous osaux4-1 or osaux4-2 exhibited shorter primary root (PR) and longer root hair (RH) compared to the wild-type Dongjin (WT/DJ), and lost response to indoleacetic acid (IAA) treatment. OsAUX4 is intensively expressed in roots and localized on the plasma membrane, suggesting that OsAUX4 might function in the regulation of root development. The decreased meristem cell division activity and the downregulated expression of cell cycle genes in root apices of osaux4 mutants supported the hypothesis that OsAUX4 positively regulates PR elongation. OsAUX4 is expressed in RH, and osaux4 mutants showing longer RH compared to WT/DJ implies that OsAUX4 negatively regulates RH development. Furthermore, osaux4 mutants are insensitive to Pi starvation (-Pi) and OsAUX4 effects on the -Pi response is associated with altered expression levels of Pi starvation-regulated genes, and auxin distribution/contents. This study revealed that OsAUX4 not only regulates PR and RH development but also plays a regulatory role in crosstalk between auxin and -Pi signaling.
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    An update on the function and regulation of methylerythritol phosphate and mevalonate pathways and their evolutionary dynamics
    Xiaojun Pu, Xiumei Dong, Qing Li, Zexi Chen and Li Liu
    J Integr Plant Biol 2021, 63 (7): 1211-1226.  
    DOI: 10.1111/jipb.13076
    Abstract (Browse 315)  |   Save
    Isoprenoids are among the largest and most chemically diverse classes of organic compounds in nature and are involved in the processes of photosynthesis, respiration, growth, development, and plant responses to stress. The basic building block units for isoprenoid synthesis—isopentenyl diphosphate and its isomer dimethylallyl diphosphate—are generated by the mevalonate (MVA) and methylerythritol phosphate (MEP) pathways. Here, we summarize recent advances on the roles of the MEP and MVA pathways in plant growth, development and stress responses, and attempt to define the underlying gene networks that orchestrate the MEP and MVA pathways in response to developmental or environmental cues. Through phylogenomic analysis, we also provide a new perspective on the evolution of the plant isoprenoid pathway. We conclude that the presence of the MVA pathway in plants may be associated with the transition from aquatic to subaerial and terrestrial environments, as lineages for its core components are absent in green algae. The emergence of the MVA pathway has acted as a key evolutionary event in plants that facilitated land colonization and subsequent embryo development, as well as adaptation to new and varied environments.
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    MP3RNA-seq: Massively parallel 3′ end RNA sequencing for high-throughput gene expression profiling and genotyping
    Jian Chen, Xiangbo Zhang, Fei Yi, Xiang Gao, Weibin Song, Haiming Zhao and Jinsheng Lai
    J Integr Plant Biol 2021, 63 (7): 1227-1239.  
    doi: 10.1111/jipb.13077
    Abstract (Browse 286)  |   Save
    Transcriptome deep sequencing (RNA-seq) has become a routine method for global gene expression profiling. However, its application to large-scale experiments remains limited by cost and labor constraints. Here we describe a massively parallel 3′ end RNA-seq (MP3RNA-seq) method that introduces unique sample barcodes during reverse transcription to permit sample pooling immediately following this initial step. MP3RNA-seq allows for handling of hundreds of samples in a single experiment, at a cost of about $6 per sample for library construction and sequencing. MP3RNA-seq is effective for not only high-throughput gene expression profiling, but also genotyping. To demonstrate its utility, we applied MP3RNA-seq to 477 double haploid lines of maize. We identified 19,429 genes expressed in at least 50% of the lines and 35,836 high-quality single nucleotide polymorphisms for genotyping analysis. Armed with these data, we performed expression and agronomic trait quantitative trait locus (QTL) mapping and identified 25,797 expression QTLs for 15,335 genes and 21 QTLs for plant height, ear height, and relative ear height. We conclude that MP3RNA-seq is highly reproducible, accurate, and sensitive for high-throughput gene expression profiling and genotyping, and should be generally applicable to most eukaryotic species.
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    The Phytophthora effector Avh241 interacts with host NDR1-like proteins to manipulate plant immunity
    Bo Yang, Sen Yang, Baodian Guo, Yuyin Wang, Wenyue Zheng, Mengjun Tian, Kaixin Dai, Zehan Liu, Haonan Wang, Zhenchuan Ma, Yan Wang, Wenwu Ye, Suomeng Dong and Yuanchao Wang
    J Integr Plant Biol 2021, 63 (7): 1382-1396.  
    DOI: 10.1111/jipb.13082
    Abstract (Browse 330)  |   Save
    Plant pathogens rely on effector proteins to suppress host innate immune responses and facilitate colonization. Although the Phytophthora sojae RxLR effector Avh241 promotes Phytophthora infection, the molecular basis of Avh241 virulence remains poorly understood. Here we identified non-race specific disease resistance 1 (NDR1)-like proteins, the critical components in plant effector-triggered immunity (ETI) responses, as host targets of Avh241. Avh241 interacts with NDR1 in the plasma membrane and suppresses NDR1-participated ETI responses. Silencing of GmNDR1s increases the susceptibility of soybean to P. sojae infection, and overexpression of GmNDR1s reduces infection, which supports its positive role in plant immunity against P. sojae. Furthermore, we demonstrate that GmNDR1 interacts with itself, and Avh241 probably disrupts the self-association of GmNDR1. These data highlight an effective counter-defense mechanism by which a Phytophthora effector suppresses plant immune responses, likely by disturbing the function of NDR1 during infection.
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    Ethylene-induced stomatal closure is mediated via MKK1/3–MPK3/6 cascade to EIN2 and EIN3
    Teng‐Yue Zhang, Zhong‐Qi Li, Yu‐Dong Zhao, Wen‐Jie Shen, Meng‐Shu Chen, Hai‐Quan Gao, Xiao‐Min Ge, Hui‐Qin Wang, Xue Li and Jun‐Min He
    J Integr Plant Biol 2021, 63 (7): 1324-1340.  
    DOI: 10.1111/jipb.13083
    Abstract (Browse 336)  |   Save
    Mitogen-activated protein kinases (MPKs) play essential roles in guard cell signaling, but whether MPK cascades participate in guard cell ethylene signaling and interact with hydrogen peroxide (H2O2), nitric oxide (NO), and ethylene-signaling components remain unclear. Here, we report that ethylene activated MPK3 and MPK6 in the leaves of wild-type Arabidopsis thaliana as well as ethylene insensitive2 (ein2), ein3, nitrate reductase1 (nia1), and nia2 mutants, but this effect was impaired in ethylene response1 (etr1), nicotinamide adenine dinucleotide phosphate oxidase AtrbohF, mpk kinase1 (mkk1), and mkk3 mutants. By contrast, the constitutive triple response1 (ctr1) mutant had constitutively active MPK3 and MPK6. Yeast two-hybrid, bimolecular fluorescence complementation, and pull-down assays indicated that MPK3 and MPK6 physically interacted with MKK1, MKK3, and the C-terminal region of EIN2 (EIN2 CEND). mkk1, mkk3, mpk3, and mpk6 mutants had typical levels of ethylene-induced H2O2 generation but impaired ethylene-induced EIN2 CEND cleavage and nuclear translocation, EIN3 protein accumulation, NO production in guard cells, and stomatal closure. These results show that the MKK1/3–MPK3/6 cascade mediates ethylene-induced stomatal closure by functioning downstream of ETR1, CTR1, and H2O2 to interact with EIN2, thereby promoting EIN3 accumulation and EIN3-dependent NO production in guard cells.
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    From genes to networks: The genetic control of leaf development
    Hongfeng Wang, Fanjiang Kong and Chuanen Zhou
    J Integr Plant Biol 2021, 63 (7): 1181-1196.  
    doi: 10.1111/jipb.13084
    Abstract (Browse 357)  |   Save
    Substantial diversity exists for both the size and shape of the leaf, the main photosynthetic organ of flowering plants. The two major forms of leaf are simple leaves, in which the leaf blade is undivided, and compound leaves, which comprise several leaflets. Leaves form at the shoot apical meristem from a group of undifferentiated cells, which first establish polarity, then grow and differentiate. Each of these processes is controlled by a combination of transcriptional regulators, microRNAs and phytohormones. The present review documents recent advances in our understanding of how these various factors modulate the development of both simple leaves (focusing mainly on the model plant Arabidopsis thaliana) and compound leaves (focusing mainly on the model legume species Medicago truncatula).
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    Exploring the diversity of plant proteome
    Yanmei Chen, Yi Wang, Jun Yang, Wenbin Zhou and Shaojun Dai
    J Integr Plant Biol 2021, 63 (7): 1197-1210.  
    DOI: 10.1111/jipb.13087
    Abstract (Browse 407)  |   Save
    The tremendous functional, spatial, and temporal diversity of the plant proteome is regulated by multiple factors that continuously modify protein abundance, modifications, interactions, localization, and activity to meet the dynamic needs of plants. Dissecting the proteome complexity and its underlying genetic variation is attracting increasing research attention. Mass spectrometry (MS)-based proteomics has become a powerful approach in the global study of protein functions and their relationships on a systems level. Here, we review recent breakthroughs and strategies adopted to unravel the diversity of the proteome, with a specific focus on the methods used to analyze posttranslational modifications (PTMs), protein localization, and the organization of proteins into functional modules. We also consider PTM crosstalk and multiple PTMs temporally regulating the life cycle of proteins. Finally, we discuss recent quantitative studies using MS to measure protein turnover rates and examine future directions in the study of the plant proteome.
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    Alternative splicing of MaMYB16L regulates starch degradation in banana fruit during ripening
    Guoxiang Jiang, Dandan Zhang, Zhiwei Li, Hanzhi Liang, Rufang Deng, Xinguo Su, Yueming Jiang and Xuewu Duan
    J Integr Plant Biol 2021, 63 (7): 1341-1352.  
    DOI: 10.1111/jipb.13088
    Abstract (Browse 300)  |   Save
    The alternative splicing of select genes is an important mechanism to regulate responses to endogenous and environmental signals in plants. However, the role of alternative splicing in regulating fruit ripening remains unclear. Here, we discovered that MaMYB16L, an R1-type MYB transcription factor, undergoes alternative splicing and generates two transcripts, the full-length isoform MaMYB16L and a truncated form MaMYB16S, in banana fruit. During banana fruit ripening, the alternative splicing process intensifies with downregulated MaMYB16L and upregulated MaMYB16S. Moreover, MaMYB16L is a transcriptional repressor that directly binds with the promoters of many genes associated with starch degradation and MaDREB2, a positive ripening regulator, and represses their expression. In contrast, MaMBY16S lacks a DNA-binding domain but competitively combines and forms non-functional heterodimers with functional MaMYB16L. MaMYB16L-MaMYB16S heterodimers decrease the binding capacity and transrepression activity of MaMYB16L. The downregulation of MaMYB16L and the upregulation of MaMYB16S, that is, a decreased ratio of active to non-active isoforms, facilitates the activation of ripening-related genes and thereby promotes fruit ripening. Furthermore, the transient overexpression of MaMYB16S promotes banana fruit ripening, whereas the overexpression of MaMYB16L delays this process. Therefore, the alternative splicing of MaMYB16L might generate a self-controlled regulatory loop to regulate banana fruit ripening.
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    MiR319-targeted OsTCP21 and OsGAmyb regulate tillering and grain yield in rice
    Rongna Wang, Xiuyan Yang, Shuang Guo, Zhaohui Wang, Zhanhui Zhang and Zhongming Fang
    J Integr Plant Biol 2021, 63 (7): 1260-1272.  
    DOI: 10.1111/jipb.13097
    Abstract (Browse 380)  |   Save
    Multiple genes and microRNAs (miRNAs) improve grain yield by promoting tillering. MiR319s are known to regulate several aspects of plant development; however, whether miR319s are essential for tillering regulation remains unclear. Here, we report that miR319 is highly expressed in the basal part of rice plant at different development stages. The miR319 knockdown line Short Tandem Target Mimic 319 (STTM319) showed higher tiller bud length in seedlings under low nitrogen (N) condition and higher tiller bud number under high N condition compared with the miR319a-overexpression line. Through targets prediction, we identified OsTCP21 and OsGAmyb as downstream targets of miR319. Moreover, OsTCP21 and OsGAmyb overexpression lines and STTM319 had increased tiller bud length and biomass, whereas both were decreased in OsTCP21 and OsGAmyb knockout lines and OE319a. These data suggest that miR319 regulates rice tiller bud development and tillering through targeting OsTCP21 and OsGAmyb. Notably, the tiller number and grain yield increased in STTM319 and overexpression lines of OsTCP21 and OsGAmyb but decreased in OE319a and knockout lines of OsTCP21 and OsGAmyb. Taken together, our findings indicate that miR319s negatively affect tiller number and grain yield by targeting OsTCP21 and OsGAmyb, revealing a novel function for miR319 in rice.
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    Functional assembly of root-associated microbial consortia improves nutrient efficiency and yield in soybean
    Cunhu Wang, Yanjun Li, Mingjia Li, Kefei Zhang, Wenjing Ma, Lei Zheng, Hanyu Xu, Baofeng Cui, Ran Liu, Yongqing Yang, Yongjia Zhong and Hong Liao
    J Integr Plant Biol 2021, 63 (6): 1021-1035.  
    doi: 10.1111/jipb.13073
    Abstract (Browse 445)  |   Save
    Root-associated microbes are critical for plant growth and nutrient acquisition. However, scant information exists on optimizing communities of beneficial root-associated microbes or the mechanisms underlying their interactions with host plants. In this report, we demonstrate that root-associated microbes are critical influencers of host plant growth and nutrient acquisition. Three synthetic communities (SynComs) were constructed based on functional screening of 1,893 microbial strains isolated from root-associated compartments of soybean plants. Functional assemblage of SynComs promoted significant plant growth and nutrient acquisition under both N/P nutrient deficiency and sufficiency conditions. Field trials further revealed that application of SynComs stably and significantly promoted plant growth, facilitated N and P acquisition, and subsequently increased soybean yield. Among the tested communities, SynCom1 exhibited the greatest promotion effect, with yield increases of up to 36.1% observed in two field sites. Further RNA-seq implied that SynCom application systemically regulates N and P signaling networks at the transcriptional level, which leads to increased representation of important growth pathways, especially those related to auxin responses. Overall, this study details a promising strategy for constructing SynComs based on functional screening, which are capable of enhancing nutrient acquisition and crop yield through the activities of beneficial root-associated microbes.
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    Root developmental responses to phosphorus nutrition
    Dong Liu
    J Integr Plant Biol 2021, 63 (6): 1065-1090.  
    doi: 10.1111/jipb.13090
    Abstract (Browse 376)  |   Save
    Phosphorus is an essential macronutrient for plant growth and development. Root system architecture (RSA) affects a plant's ability to obtain phosphate, the major form of phosphorus that plants uptake. In this review, I first consider the relationship between RSA and plant phosphorus-acquisition efficiency, describe how external phosphorus conditions both induce and impose changes in the RSA of major crops and of the model plant Arabidopsis, and discuss whether shoot phosphorus status affects RSA and whether there is a universal root developmental response across all plant species. I then summarize the current understanding of the molecular mechanisms governing root developmental responses to phosphorus deficiency. I also explore the possible reasons for the inconsistent results reported by different research groups and comment on the relevance of some studies performed under laboratory conditions to what occurs in natural environments.
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    NF-YCs modulate histone variant H2A.Z deposition to regulate photomorphogenic growth in Arabidopsis
    Chunyu Zhang, Qian Qian, Xiang Huang, Wenbin Zhang, Xu Liu and Xingliang Hou
    J Integr Plant Biol 2021, 63 (6): 1120-1132.  
    DOI: 10.1111/jipb.13109
    Abstract (Browse 206)  |   Save
    In plants, light signals trigger a photomorphogenic program involving transcriptome changes, epigenetic regulation, and inhibited hypocotyl elongation. The evolutionarily conserved histone variant H2A.Z, which functions in transcriptional regulation, is deposited in chromatin by the SWI2/SNF2-RELATED 1 complex (SWR1c). However, the role of H2A.Z in photomorphogenesis and its deposition mechanism remain unclear. Here, we show that in Arabidopsis thaliana, H2A.Z deposition at its target loci is induced by light irradiation via NUCLEAR FACTOR-Y, subunit C (NF-YC) proteins, thereby inhibiting photomorphogenic growth. NF-YCs physically interact with ACTIN-RELATED PROTEIN6 (ARP6), a key component of the SWR1c that is essential for depositing H2A.Z, in a light-dependent manner. NF-YCs and ARP6 function together as negative regulators of hypocotyl growth by depositing H2A.Z at their target genes during photomorphogenesis. Our findings reveal an important role for the histone variant H2A.Z in photomorphogenic growth and provide insights into a novel transcription regulatory node that mediates H2A.Z deposition to control plant growth in response to changing light conditions.
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    The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis
    Lin‐Lin Zhang, Wei Li, Ying‐Ying Tian, Seth Jon Davis and Jian‐Xiang Liu
    J Integr Plant Biol 2021, 63 (6): 1097-1103.  
    doi: 10.1111/jipb.13107
    Abstract (Browse 321)  |   Save
    Plants are capable of coordination of their growth and development with ambient temperatures. EARLY FLOWERING3 (ELF3), an essential component of the plant circadian clock, is also involved in ambient temperature sensing, as well as in inhibiting the expression and protein activity of the thermoresponsive regulator phytochrome interacting factor 4 (PIF4). The ELF3 activity is subjected to attenuation in response to warm temperature; however, how the protein level of ELF3 is regulated at warm temperature remains less understood. Here, we report that the E3 ligase XB3 ORTHOLOG 5 IN ARABIDOPSIS THALIANA, XBAT35, mediates ELF3 degradation. XBAT35 interacts with ELF3 and ubiquitinates ELF3. Loss-of-function mutation of XBAT35 increases the protein level of ELF3 and confers a short-hypocotyl phenotype under warm temperature conditions. Thus, our findings establish that XBAT35 mediates ELF3 degradation to lift the inhibition of ELF3 on PIF4 for promoting thermoresponsive hypocotyl growth in plants.
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    Phytochrome B interacts with SWC6 and ARP6 to regulate H2A.Z deposition and photomorphogensis in Arabidopsis
    Xuxu Wei, Wanting Wang, Peng Xu, Wenxiu Wang, Tongtong Guo, Shuang Kou, Minqing Liu, Yake Niu, Hong‐Quan Yang and Zhilei Mao
    J Integr Plant Biol 2021, 63 (6): 1133-1146.  
    DOI: 10.1111/jipb.13111
    Abstract (Browse 259)  |   Save
    Light serves as a crucial environmental cue which modulates plant growth and development, and which is controlled by multiple photoreceptors including the primary red light photoreceptor, phytochrome B (phyB). The signaling mechanism of phyB involves direct interactions with a group of basic helix-loop-helix (bHLH) transcription factors, PHYTOCHROME-INTERACTING FACTORS (PIFs), and the negative regulators of photomorphogenesis, COP1 and SPAs. H2A.Z is an evolutionarily conserved H2A variant which plays essential roles in transcriptional regulation. The replacement of H2A with H2A.Z is catalyzed by the SWR1 complex. Here, we show that the Pfr form of phyB physically interacts with the SWR1 complex subunits SWC6 and ARP6. phyB and ARP6 co-regulate numerous genes in the same direction, some of which are associated with auxin biosynthesis and response including YUC9, which encodes a rate-limiting enzyme in the tryptophan-dependent auxin biosynthesis pathway. Moreover, phyB and HY5/HYH act to inhibit hypocotyl elongation partially through repression of auxin biosynthesis. Based on our findings and previous studies, we propose that phyB promotes H2A.Z deposition at YUC9 to inhibit its expression through direct phyB-SWC6/ARP6 interactions, leading to repression of auxin biosynthesis, and thus inhibition of hypocotyl elongation in red light.
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    HBI1‐TCP20 interaction positively regulates the CEPs‐mediated systemic nitrate acquisition
    Xiaoqian Chu, Mingzhe Li, Shujuan Zhang, Min Fan, Chao Han, Fengning Xiang, Genying Li, Yong Wang, Cheng‐Bin Xiang, Jia‐Gang Wang and Ming‐Yi Bai
    J Integr Plant Biol 2021, 63 (5): 902-912.  
    DOI: 10.1111/jipb.13035
    Abstract (Browse 282)  |   Save
    Nitrate is the main source of nitrogen for plants but often distributed heterogeneously in soil. Plants have evolved sophisticated strategies to achieve adequate nitrate by modulating the root system architecture. The nitrate acquisition system is triggered by the short mobile peptides C‐TERMINALLY ENCODED PEPTIDES (CEPs) that are synthesized on the nitrate‐starved roots, but induce the expression of nitrate transporters on the other nitrate‐rich roots through an unclear signal transduction pathway. Here, we demonstrate that the transcription factors HBI1 and TCP20 play important roles in plant growth and development in response to fluctuating nitrate supply. HBI1 physically interacts with TCP20, and this interaction was enhanced by the nitrate starvation. HBI1 and TCP20 directly bind to the promoters of CEPs and cooperatively induce their expression. Mutation in HBIs and/or TCP20 resulted in impaired systemic nitrate acquisition response. Our solid genetic and molecular evidence strongly indicate that the HBI1‐TCP20 module positively regulates the CEPs‐mediated systemic nitrate acquisition.
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    The NPR1‐WRKY46‐WRKY6 signaling cascade mediates probenazole/salicylic acid‐elicited leaf senescence in Arabidopsis thaliana
    Dingyu Zhang, Zheng Zhu, Jiong Gao, Xin Zhou, Shuai Zhu, Xiaoyan Wang, Xiaolei Wang, Guodong Ren and Benke Kuai
    J Integr Plant Biol 2021, 63 (5): 924-936.  
    DOI: 10.1111/jipb.13044
    Abstract (Browse 444)  |   Save
    Endogenous salicylic acid (SA) regulates leaf senescence, but the underlying mechanism remains largely unexplored. The exogenous application of SA to living plants is not efficient for inducing leaf senescence. By taking advantage of probenazole (PBZ)‐induced biosynthesis of endogenous SA, we previously established a chemical inducible leaf senescence system that depends on SA biosynthesis and its core signaling receptor NPR1 in Arabidopsis thaliana. Here, using this system, we identified WRKY46 and WRKY6 as key components of the transcriptional machinery downstream of NPR1 signaling. Upon PBZ treatment, the wrky46 mutant exhibited significantly delayed leaf senescence. We demonstrate that NPR1 is essential for PBZ/SA‐induced WRKY46 activation, whereas WRKY46 in turn enhances NPR1 expression. WRKY46 interacts with NPR1 in the nucleus, binding to the W‐box of the WRKY6 promoter to induce its expression in response to SA signaling. Dysfunction of WRKY6 abolished PBZ‐induced leaf senescence, while overexpression of WRKY6 was sufficient to accelerate leaf senescence even under normal growth conditions, suggesting that WRKY6 may serve as an integration node of multiple leaf senescence signaling pathways. Taken together, these findings reveal that the NPR1‐WRKY46‐WRKY6 signaling cascade plays a critical role in PBZ/SA‐mediated leaf senescence in Arabidopsis.
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    Rice FLOURY ENDOSPERM 18 encodes a pentatricopeptide repeat protein required for 5′ processing of mitochondrial nad5 messenger RNA and endosperm development
    Mingzhou Yu, Mingming Wu, Yulong Ren, Yihua Wang, Jingfang Li, Cailin Lei, Yinglun Sun, Xiuhao Bao, Hongming Wu, Hang Yang, Tian Pan, Yongfei Wang, Ruonan Jing, Mengyuan Yan, Houda Zhang, Lei Zhao, Zhichao Zhao, Xin Zhang, Xiuping Guo, Zhijun Cheng, Bing Yang, Ling Jiang and Jianmin Wan
    J Integr Plant Biol 2021, 63 (5): 834-847.  
    DOI: 10.1111/jipb.13049
    Abstract (Browse 449)  |   Save
    Pentatricopeptide repeat (PPR) proteins, composing one of the largest protein families in plants, are involved in RNA binding and regulation of organelle RNA metabolism at the post‐transcriptional level. Although several PPR proteins have been implicated in endosperm development in rice (Oryza sativa), the molecular functions of many PPRs remain obscure. Here, we identified a rice endosperm mutant named floury endosperm 18 (flo18) with pleiotropic defects in both reproductive and vegetative development. Map‐based cloning and complementation tests showed that FLO18 encodes a mitochondrion‐targeted P‐type PPR protein with 15 PPR motifs. Mitochondrial function was disrupted in the flo18 mutant, as evidenced by decreased assembly of Complex I in the mitochondrial electron transport chain and altered mitochondrial morphology. Loss of FLO18 function resulted in defective 5′‐end processing of mitochondrial nad5 transcripts encoding subunit 5 of nicotinamide adenine dinucleotide hydrogenase. These results suggested that FLO18 is involved in 5′‐end processing of nad5 messenger RNA and plays an important role in mitochondrial function and endosperm development.
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    Induction of jasmonic acid biosynthetic genes inhibits Arabidopsis growth in response to low boron
    Yupu Huang, Sheliang Wang, Chuang Wang, Guangda Ding, Hongmei Cai, Lei Shi and Fangsen Xu
    J Integr Plant Biol 2021, 63 (5): 937-948.  
    doi: 10.1111/jipb.13048
    Abstract (Browse 309)  |   Save
    The essential micronutrient boron (B) has key roles in cell wall integrity and B deficiency inhibits plant growth. The role of jasmonic acid (JA) in plant growth inhibition under B deficiency remains unclear. Here, we report that low B elevates JA biosynthesis in Arabidopsis thaliana by inducing the expression of JA biosynthesis genes. Treatment with JA inhibited plant growth and, a JA biosynthesis inhibitor enhanced plant growth, indicating that the JA induced by B deficiency affects plant growth. Furthermore, examination of the JA signaling mutants jasmonate resistant1, coronatine insensitive1‐2, and myc2 showed that JA signaling negatively regulates plant growth under B deficiency. We identified a low‐B responsive transcription factor, ERF018, and used yeast one‐hybrid assays and transient activation assays in Nicotiana benthamiana leaf cells to demonstrate that ERF018 activates the expression of JA biosynthesis genes. ERF018 overexpression (OE) lines displayed stunted growth and up‐regulation of JA biosynthesis genes under normal B conditions, compared to Col‐0 and the difference between ERF018 OE lines and Col‐0 diminished under low B. These results suggest that ERF018 enhances JA biosynthesis and thus negatively regulates plant growth. Taken together, our results highlight the importance of JA in the effect of low B on plant growth.
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    BRITTLE PLANT1 is required for normal cell wall composition and mechanical strength in rice
    Yuanyan Zhang, Yihua Wang, Chunming Wang, Carsten Rautengarten, Erchao Duan, Jianping Zhu, Xiaopin Zhu, Jie Lei, Chao Peng, Yunlong Wang, Xuan Teng, Yunlu Tian, Xi Liu, Joshua L. Heazlewood, Aimin Wu and Jianmin Wan
    J Integr Plant Biol 2021, 63 (5): 865-877.  
    DOI: 10.1111/jipb.13050
    Abstract (Browse 356)  |   Save
    A series of nucleotide sugar interconversion enzymes (NSEs) generate the activated sugar donors required for biosynthesis of cell wall matrix polysaccharides and glycoproteins. UDP‐glucose 4‐epimerases (UGEs) are NSEs that function in the interconversion of UDP‐glucose (UDP‐Glc) and UDP‐galactose (UDP‐Gal). The roles of UDP‐glucose 4‐epimerases in monocots remain unclear due to redundancy in the pathways. Here, we report a brittle plant (bp1) rice mutant that exhibits brittle leaves and culms at all growth stages. The mutant culms had reduced levels of rhamnogalacturonan I, homogalacturonan, and arabinogalactan proteins. Moreover, the mutant had altered contents of uronic acids, neutral noncellulosic monosaccharides, and cellulose. Map‐based cloning demonstrated that OsBP1 encodes a UDP‐glucose 4‐epimerase (OsUGE2), a cytosolic protein. We also show that BP1 can form homo‐ and hetero‐protein complexes with other UGE family members and with UDP‐galactose transporters 2 (OsUGT2) and 3 (OsUGT3), which may facilitate the channeling of Gal to polysaccharides and proteoglycans. Our results demonstrate that BP1 participates in regulating the sugar composition and structure of rice cell walls.
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    A rice tubulin tyrosine ligase‐like 12 protein affects the dynamic and orientation of microtubules
    Kunxi Zhang, Xin Zhu, Steffen Durst, Petra Hohenberger, Min‐Jung Han, Gynheung An, Vaidurya P. Sahi, Michael Riemann and Peter Nick
    J Integr Plant Biol 2021, 63 (5): 848-864.  
    doi: 10.1111/jipb.13059
    Abstract (Browse 234)  |   Save
    The detyrosination/retyrosination cycle is the most common post‐translational modification of α‐tubulin. Removal of the conserved C‐terminal tyrosine of α‐tubulin by a still elusive tubulin tyrosine carboxypeptidase, and religation of this tyrosine by a tubulin tyrosine ligase (TTL), are probably common to all eukaryotes. Interestingly, for plants, the only candidates qualifying as potential TTL homologs are the tubulin tyrosine ligase‐like 12 proteins. To get insight into the biological functions of these potential TTL homologs, we cloned the rice TTL‐like 12 protein (OsTTLL12) and generated overexpression OsTTLL12‐RFP lines in both rice and tobacco BY‐2 cells. We found, unexpectedly, that overexpression of this OsTTLL12‐RFP increased the relative abundance of detyrosinated α‐tubulin in both coleoptile and seminal root, correlated with more stable microtubules. This was independent of the respective orientation of cortical microtubule, and followed by correspondingly changing growth of coleoptiles and seminal roots. A perturbed organization of phragmoplast microtubules and disoriented cell walls were further characteristics of this phenotype. Thus, the elevated tubulin detyrosination in consequence of OsTTLL12 overexpression affects structural and dynamic features of microtubules, followed by changes in the axiality of cell plate deposition and, consequently, plant growth.
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    Salicylic acid and ethylene coordinately promote leaf senescence
    Xiaodong Yu, Yiren Xu and Shunping Yan
    J Integr Plant Biol 2021, 63 (5): 823-827.  
    doi: 10.1111/jipb.13074
    Abstract (Browse 441)  |   Save
    Leaf senescence is an intrinsic biological process of plants. The phytohormones salicylic acid (SA) and ethylene (ET) are known to promote senescence. However, their relationship in this process is still unclear. We found that EIN3 and EIL1, two key transcription factors in ET signaling, are required for SA‐induced leaf senescence in Arabidopsis. Furthermore, ET enhances the effect of SA in promoting senescence. Biochemical studies revealed that NPR1, the master regulator of SA signaling, interacts with EIN3 to promote its transcriptional activity. Our study suggests that SA and ET function coordinately in senescence, which is in contrast to their antagonistic crosstalk in other biological processes.
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    Ethylene and salicylic acid synergistically accelerate leaf senescence in Arabidopsis
    Chaoqi Wang, Shouyi Dai, Zhong‐Lin Zhang, Wenqing Lao, Ruiying Wang, Xianqing Meng and Xin Zhou
    J Integr Plant Biol 2021, 63 (5): 828-833.  
    doi: 10.1111/jipb.13075
    Abstract (Browse 455)  |   Save
    The phytohormones ethylene and salicylic acid (SA) have long been known to promote senescence, but their interplay during this process remains elusive. Here we report the synergistic effects of ethylene and SA on promoting leaf senescence in Arabidopsis. EIN3, a key transcription factor of ethylene signaling, physically interacted with the core SA signaling regulator NPR1 in senescing leaves. EIN3 and NPR1 synergistically promoted the expression of the senescence‐associated genes ORE1 and SAG29. The senescence phenotype was more delayed for the ein3eil1npr1 triple mutant than ein3eil1 or npr1 with ethylene or/and SA treatment. NPR1‐promoted leaf senescence may depend on functional EIN3/EIL1.
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    ABNORMAL SHOOT 6 interacts with KATANIN 1 and SHADE AVOIDANCE 4 to promote cortical microtubule severing and ordering in Arabidopsis
    Yuanfeng Li, Meng Deng, Haofeng Liu, Yan Li, Yu Chen, Min Jia, Hui Xue, Jingxia Shao, Jun Zhao, Yafei Qi, Lijun An, Fei Yu and Xiayan Liu
    J Integr Plant Biol 2021, 63 (4): 646-661.  
    DOI: 10.1111/jipb.13003
    Abstract (Browse 422)  |   Save
    Plant interphase cortical microtubules (cMTs) mediate anisotropic cell expansion in response to environmental and developmental cues. In Arabidopsis thaliana, KATANIN 1 (KTN1), the p60 catalytic subunit of the conserved MT‐severing enzyme katanin, is essential for cMT ordering and anisotropic cell expansion. However, the regulation of KTN1‐mediated cMT severing and ordering remains unclear. In this work, we report that the Arabidopsis IQ67 DOMAIN (IQD) family gene ABNORMAL SHOOT 6 (ABS6) encodes a MT‐associated protein. Overexpression of ABS6 leads to elongated cotyledons, directional pavement cell expansion, and highly ordered transverse cMT arrays. Genetic suppressor analysis revealed that ABS6‐mediated cMT ordering is dependent on KTN1 and SHADE AVOIDANCE 4 (SAV4). Live imaging of cMT dynamics showed that both ABS6 and SAV4 function as positive regulators of cMT severing. Furthermore, ABS6 directly interacts with KTN1 and SAV4 and promotes their recruitment to the cMTs. Finally, analysis of loss‐of‐function mutant combinations showed that ABS6, SAV4, and KTN1 work together to ensure the robust ethylene response in the apical hook of dark‐grown seedlings. Together, our findings establish ABS6 and SAV4 as positive regulators of cMT severing and ordering, and highlight the role of cMT dynamics in fine‐tuning differential growth in plants.
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    The Arabidopsis R‐SNARE protein YKT61 is essential for gametophyte development
    Ting Ma, En Li, Lu‐Shen Li, Sha Li and Yan Zhang
    J Integr Plant Biol 2021, 63 (4): 676-694.  
    DOI: 10.1111/jipb.13017
    Abstract (Browse 460)  |   Save
    Gametophyte development is a pre‐requisite for plant reproduction and seed yield; therefore, studies of gametophyte development help us understand fundamental biological questions and have potential applications in agriculture. The biogenesis and dynamics of endomembrane compartments are critical for cell survival, and their regulatory mechanisms are just beginning to be revealed. Here, we report that the Arabidopsis thaliana SNARE (soluble N‐ethylmaleimide sensitive factor attachment protein receptor) protein YKT61 is essential for both male and female gametogenesis. By using clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR‐associated protein 9 (Cas9)‐based genome editing, we demonstrated that male and female gametophytes carrying YKT61 loss‐of‐function alleles do not survive. Specifically, loss of YKT61 function resulted in the arrest of male gametophytic development at pollen mitosis I and the degeneration of female gametophytes. A three‐base‐pair deletion in YKT61 in the ykt61‐3 mutant resulted in a single‐amino acid deletion in the longin domain of YKT61; the resulting mutant protein does not interact with multiple SNAREs and showed substantially reduced membrane association, suggesting that the N‐terminal longin domain of YKT61 plays multiple roles in its function. This study demonstrates that Arabidopsis YKT61 is essential for male and female gametogenesis and sets an example for functional characterization of essential genes with the combination of Cas9‐mediated editing and expression from a Cas9‐resistant transgene.
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    Roles of DEMETER in regulating DNA methylation in vegetative tissues and pathogen resistance
    Wenjie Zeng, Huan Huang, Xueqiang Lin, Chen Zhu, Ken‐ichi Kosami, Chaofeng Huang, Huiming Zhang, Cheng‐Guo Duan, Jian‐Kang Zhu and Daisuke Miki
    J Integr Plant Biol 2021, 63 (4): 691-706.  
    doi: 10.1111/jipb.13037
    Abstract (Browse 290)  |   Save
    DNA methylation is an epigenetic mark important for genome stability and gene expression. In Arabidopsis thaliana, the 5‐methylcytosine DNA glycosylase/demethylase DEMETER (DME) controls active DNA demethylation during the reproductive stage; however, the lethality of loss‐of‐function dme mutations has made it difficult to assess DME function in vegetative tissues. Here, we edited DME using clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR‐associated protein 9 and created three weak dme mutants that produced a few viable seeds. We also performed central cell‐specific complementation in a strong dme mutant and combined this line with mutations in the other three Arabidopsis demethylase genes to generate the dme ros1 dml2 dml3 (drdd) quadruple mutant. A DNA methylome analysis showed that DME is required for DNA demethylation at hundreds of genomic regions in vegetative tissues. A transcriptome analysis of the drdd mutant revealed that DME and the other three demethylases are important for plant responses to biotic and abiotic stresses in vegetative tissues. Despite the limited role of DME in regulating DNA methylation in vegetative tissues, the dme mutants showed increased susceptibility to bacterial and fungal pathogens. Our study highlights the important functions of DME in vegetative tissues and provides valuable genetic tools for future investigations of DNA demethylation in plants.
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    AtNSF regulates leaf serration by modulating intracellular trafficking of PIN1 in Arabidopsis thaliana
    Li Ping Tang, Yi Yang, Hui Wang, Lixin Li, Le Liu, Yu Liu, Jinfeng Yuan, Xiang Yu Zhao, Klaus Palme, Ying Hua Su and Xugang Li
    J Integr Plant Biol 2021, 63 (4): 737-755.  
    DOI: 10.1111/jipb.13043
    Abstract (Browse 274)  |   Save
    In eukaryotes, N‐ethylmaleimide‐sensitive factor (NSF) is a conserved AAA+ATPase and a key component of the membrane trafficking machinery that promotes the fusion of secretory vesicles with target membranes. Here, we demonstrate that the Arabidopsis thaliana genome contains a single copy of NSF, AtNSF, which plays an essential role in the regulation of leaf serration. The AtNSF knock‐down mutant, atnsf‐1, exhibited more serrations in the leaf margin. Moreover, polar localization of the PIN‐FORMED1 (PIN1) auxin efflux transporter was diffuse around the margins of atnsf‐1 leaves and root growth was inhibited in the atnsf‐1 mutant. More PIN1‐GFP accumulated in the intracellular compartments of atnsf‐1 plants, suggesting that AtNSF is required for intracellular trafficking of PIN between the endosome and plasma membrane. Furthermore, the serration phenotype was suppressed in the atnsf‐1 pin1‐8 double mutant, suggesting that AtNSF is required for PIN1‐mediated polar auxin transport to regulate leaf serration. The CUP‐SHAPED COTYLEDON2 (CUC2) transcription factor gene is up‐regulated in atnsf‐1 plants and the cuc2‐3 single mutant exhibits smooth leaf margins, demonstrating that AtNSF also functions in the CUC2 pathway. Our results reveal that AtNSF regulates the PIN1‐generated auxin maxima with a CUC2‐mediated feedback loop to control leaf serration.
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    Maize endosperm development
    Dawei Dai, Zeyang Ma and Rentao Song
    J Integr Plant Biol 2021, 63 (4): 613-627.  
    doi: 10.1111/jipb.13069
    Abstract (Browse 423)  |   Save
    Recent breakthroughs in transcriptome analysis and gene characterization have provided valuable resources and information about the maize endosperm developmental program. The high temporal‐resolution transcriptome analysis has yielded unprecedented access to information about the genetic control of seed development. Detailed spatial transcriptome analysis using laser‐capture microdissection has revealed the expression patterns of specific populations of genes in the four major endosperm compartments: the basal endosperm transfer layer (BETL), aleurone layer (AL), starchy endosperm (SE), and embryo‐surrounding region (ESR). Although the overall picture of the transcriptional regulatory network of endosperm development remains fragmentary, there have been some exciting advances, such as the identification of OPAQUE11 (O11) as a central hub of the maize endosperm regulatory network connecting endosperm development, nutrient metabolism, and stress responses, and the discovery that the endosperm adjacent to scutellum (EAS) serves as a dynamic interface for endosperm‐embryo crosstalk. In addition, several genes that function in BETL development, AL differentiation, and the endosperm cell cycle have been identified, such as ZmSWEET4c, Thk1, and Dek15, respectively. Here, we focus on current advances in understanding the molecular factors involved in BETL, AL, SE, ESR, and EAS development, including the specific transcriptional regulatory networks that function in each compartment during endosperm development.
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    N4‐methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis
    Le Nguyen Tieu Ngoc, Su Jung Park, Trinh Thi Huong, Kwang Ho Lee and Hunseung Kang
    J Integr Plant Biol 2021, 63 (3): 570-582.  
    doi: 10.1111/jipb.13009
    Abstract (Browse 301)  |   Save
    Although the essential role of messenger RNA methylation in the nucleus is increasingly understood, the nature of ribosomal RNA (rRNA) methyltransferases and the role of rRNA methylation in chloroplasts remain largely unknown. A recent study revealed that CMAL (for Chloroplast mr aW‐ Like) is a chloroplast‐localized rRNA methyltransferase that is responsible for N4‐methylcytidine (m4C) in 16S chloroplast rRNA in Arabidopsis thaliana. In this study, we further examined the role of CMAL in chloroplast biogenesis and function, development, and hormone response. The cmal mutant showed reduced chlorophyll biosynthesis, photosynthetic activity, and growth‐defect phenotypes, including severely stunted stems, fewer siliques, and lower seed yield. The cmal mutant was hypersensitive to chloroplast translation inhibitors, such as lincomycin and erythromycin, indicating that the m4C‐methylation defect in the 16S rRNA leads to a reduced translational activity in chloroplasts. Importantly, the stunted stem of the cmal mutant was partially rescued by exogenous gibberellic acid or auxin. The cmal mutant grew poorer than wild type, whereas the CMAL‐overexpressing transgenic Arabidopsis plants grew better than wild type in the presence of abscisic acid. Altogether, these results indicate that CMAL is an indispensable rRNA methyltransferase in chloroplasts and is crucial for chloroplast biogenesis and function, photosynthesis, and hormone response during plant growth and development.
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    Salicylic acid promotes quiescent center cell division through ROS accumulation and down‐regulation of PLT1, PLT2, and WOX5
    Zhuqing Wang, Duoyan Rong, Dixing Chen, Yang Xiao, Renyi Liu, Shuang Wu and Chizuko Yamamuro
    J Integr Plant Biol 2021, 63 (3): 583-596.  
    doi: 10.1111/jipb.13020
    Abstract (Browse 436)  |   Save
    Salicylic acid (SA) plays a crucial role in plant immunity. However, its function in plant development is poorly understood. The quiescent center (QC), which maintains columella stem cells (CSCs) in the root apical meristem and typically exhibits low levels of cell division, is critical for root growth and development. Here, we show that the Arabidopsis thaliana SA overaccumulation mutant constitutively activated cell death 1 (cad1), which exhibits increased cell division in the QC, is rescued by additional mutations in genes encoding the SA biosynthetic enzyme SALICYLIC ACID INDUCTION DEFFICIENT2 (SID2) or the SA receptor NONEXPRESSER OF PR GENES1 (NPR1), indicating that QC cell division in the cad1 mutant is promoted by the NPR1‐dependent SA signaling pathway. The application of exogenous SA also promoted QC cell division in wild‐type plants in a dose‐dependent manner and largely suppressed the expression of genes involved in QC maintenance, including those encoding the APETALA2 (AP2) transcription factors PLETHORA1 (PLT1) and PLT2, as well as the homeodomain transcription factor WUSCHEL‐RELATED HOMEOBOX5 (WOX5). Moreover, we showed that SA promotes reactive oxygen species (ROS) production, which is necessary for the QC cell division phenotype in the cad1 mutant. These results provide insight into the function of SA in QC maintenance.
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    Abscisic acid receptors maintain abscisic acid homeostasis by modulating UGT71C5 glycosylation activity
    Yanlin Ma, Jing Cao, Qiaoqiao Chen, Jiahan He, Zhibin Liu, Jianmei Wang, Xufeng Li and Yi Yang
    J Integr Plant Biol 2021, 63 (3): 543-552.  
    doi: 10.1111/jipb.13030
    Abstract (Browse 377)  |   Save
    Uridine diphosphate‐glucosyltransferases (UGTs) maintain abscisic acid (ABA) homeostasis in Arabidopsis thaliana by converting ABA to abscisic acid‐glucose ester (ABA‐GE). UGT71C5 plays an important role in the generation of ABA‐GE. Abscisic acid receptors are crucial upstream components of the ABA signaling pathway, but how UGTs and ABA receptors function together to modulate ABA levels is unknown. Here, we demonstrated that the ABA receptors RCAR12/13 and UGT71C5 maintain ABA homeostasis in Arabidopsis following rehydration under drought stress. Biochemical analyses show that UGT71C5 directly interacted with RCAR8/12/13 in yeast cells, and the interactions between UGT71C5 and RCAR12/13 were enhanced by ABA treatment. Enzyme activity analysis showed that ABA‐GE contents were significantly elevated in the presence of RCAR12 or RCAR13, suggesting that these ABA receptors enhance the activity of UGT71C5. Determination of the content of ABA and ABA‐GE in Arabidopsis following rehydration under drought stress revealed that ABA‐GE contents were significantly higher in Arabidopsis plants overexpressing RCAR12 and RCAR13 than in non‐transformed plants and plants overexpressing RCAR11 following rehydration under drought stress. These observations suggest that RCAR12 and RCAR13 enhance the activity of UGT71C5 to glycosylate excess ABA into ABA‐GE following rehydration under drought stress, representing a rapid mechanism for regulating plant growth and development.
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    Abscisic acid signaling negatively regulates nitrate uptake via phosphorylation of NRT1.1 by SnRK2s in Arabidopsis
    Hang Su, Tian Wang, Chuanfeng Ju, Jinping Deng, Tianqi Zhang, Mengjiao Li, Hui Tian and Cun Wang
    J Integr Plant Biol 2021, 63 (3): 597-610.  
    doi: 10.1111/jipb.13057
    Abstract (Browse 537)  |   Save
    Nitrogen (N) is a limiting nutrient for plant growth and productivity. The phytohormone abscisic acid (ABA) has been suggested to play a vital role in nitrate uptake in fluctuating N environments. However, the molecular mechanisms underlying the involvement of ABA in N deficiency responses are largely unknown. In this study, we demonstrated that ABA signaling components, particularly the three subclass III SUCROSE NON‐FERMENTING1 (SNF1)‐RELATED PROTEIN KINASE 2S (SnRK2) proteins, function in root foraging and uptake of nitrate under N deficiency in Arabidopsis thaliana. The snrk2.2snrk2.3snrk2.6 triple mutant grew a longer primary root and had a higher rate of nitrate influx and accumulation compared with wild‐type plants under nitrate deficiency. Strikingly, SnRK2.2/2.3/2.6 proteins interacted with and phosphorylated the nitrate transceptor NITRATE TRANSPORTER1.1 (NRT1.1) in vitro and in vivo. The phosphorylation of NRT1.1 by SnRK2s resulted in a significant decrease of nitrate uptake and impairment of root growth. Moreover, we identified NRT1.1Ser585 as a previously unknown functional site: the phosphomimetic NRT1.1S585D was impaired in both low‐ and high‐affinity transport activities. Taken together, our findings provide new insight into how plants fine‐tune growth via ABA signaling under N deficiency.
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    Fig fruit ripening is regulated by the interaction between ethylene and abscisic acid
    Han Qiao, Han Zhang, Zhun Wang and Yuanyue Shen
    J Integr Plant Biol 2021, 63 (3): 553-569.  
    doi: 10.1111/jipb.13065
    Abstract (Browse 313)  |   Save
    Fleshy fruit ripening is typically regulated by ethylene in climacteric fruits and abscisic acid (ABA) in non‐climacteric fruits. Common fig (Ficus carica) shows a dual‐ripening mechanism, which is not fully understood. Here, we detected separate peaks of ethylene and ABA in fig fruits at the onset‐ and on‐ripening stages, in conjunction with a sharp rise in glucose and fructose contents. In a newly‐designed split‐fruit system, exogenous ethylene failed to rescue fluridone‐inhibited fruit ripening, whereas exogenous ABA rescued 2‐amino‐ethoxy‐vinyl glycine (AVG)‐inhibited fruit ripening. Transcriptome analysis revealed changes in the expression of genes key to both ABA and ethylene biosynthesis and perception during fig fruit ripening. At the de‐greening stage, downregulation of FcACO2 or FcPYL8 retarded ripening, but downregulation of FcETR1/2 did not; unexpectedly, downregulation of FcAAO3 promoted ripening, but it inhibited ripening only before the de‐greening stage. Furthermore, we detected an increase in ethylene emissions in the FcAAO3‐RNAi ripening fruit and a decrease in ABA levels in the FcACO2‐RNAi unripening fruit. Importantly, FcPYL8 can bind to ABA, suggesting that it functions as an ABA receptor. Our findings support the hypothesis that ethylene regulates the fig fruit ripening in an ABA‐dependent manner. We propose a model for the role of the ABA–ethylene interaction in climacteric/non‐climacteric processes.
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