Hormone signaling

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    Rice miR394 suppresses leaf inclination through targeting an F-box gene, LEAF INCLINATION 4
    Li Qu, Li-Bi Lin and Hong-Wei Xue
    J Integr Plant Biol 2019, 61 (4): 406-416.  
    DOI: 10.1111/jipb.12713
    Abstract (Browse 311)  |   Save
    Rice leaf inclination is an important agronomic trait, closely related to plant architecture and yield. Identification of genes controlling leaf inclination would assist in crop improvement. Although various factors, including the plant hormones auxin and brassinosteroids, have been shown to regulate lamina joint development, the role of microRNAs in regulating leaf inclination remains largely unknown. Here, we functionally characterize the role of rice miR394 and its target, LEAF INCLINCATION 4 (LC4), which encodes an F-box protein, in the regulation of leaf inclination. We show that miR394 and LC4 work, antagonistically, to regulate leaf lamina joint development and rice architecture, by modulating expansion and elongation of adaxial parenchyma cells. Suppressed expression of miR394, or enhanced expression of LC4, results in enlarged leaf angles, whereas reducing LC4 expression by CRISPR/Cas9 leads to reduced leaf inclination, suggesting LC4 as candidate for use in rice architecture improvement. LC4 interacts with SKP1, a component of the SCF E3 ubiquitin ligase complex, and transcription of both miR394 and LC4 are regulated by auxin. Rice plants with altered expression of miR394 or LC4 have altered auxin responses, indicating that the miR394-LC4 module mediates auxin effects important for determining rice leaf inclination and architecture.
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    Arabidopsis ANAC092 regulates auxin-mediated root development by binding to the ARF8 and PIN4 promoters
    Dandan Xi, Xu Chen, Yuxia Wang, Ruiling Zhong, Jianmei He, Jiabin Shen and Feng Ming
    J Integr Plant Biol 2019, 61 (9): 1015-1031.  
    DOI: 10.1111/jipb.12735
    Abstract (Browse 746)  |   Save

    Auxin is an important plant hormone that is essential for growth and development due to its effects on organogenesis, morphogenesis, tropisms, and apical dominance. The functional diversity of auxin highlights the importance of its biosynthesis, transport, and associated responses. In this study, we show that a NAC transcription factor, ANAC092 (also named AtNAC2 and ORESARA1), known to positively regulate leaf senescence and contribute to abiotic stress responses, also affects primary root development. Plants overexpressing ANAC092 had altered root meristem lengths and shorter primary roots compared with the wild‐type control. Additionally, expression of the proANAC092::GUS was strongly induced by indole‐3‐acetic acid. Quantitative real‐time RT‐PCR (qRT‐PCR) analysis revealed that the YUCCA2, PIN, and ARF expression levels were downregulated in ANAC092‐overexpressing plants. Moreover, yeast one‐hybrid and chromatin immunoprecipitation assays confirmed that ANAC092 binds to the promoters of AUXIN RESPONSE FACTOR 8 (ARF8) and PIN‐FORMED 4 (PIN4). Furthermore, a dual‐luciferase assay indicated that ANAC092 decreases ARF8 and PIN4 promoter activities. We also applied a CRISPR/Cas9 system to mutate ANAC092. The roots of three of the analyzed mutants were longer than normal. Collectively, our findings indicate that ANAC092 negatively affects root development by controlling the auxin pathway.

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    Gibberellin repression of axillary bud formation in Arabidopsis by modulation of DELLA-SPL9 complex activity
    Qi-Qi Zhang, Jia-Gang Wang, Ling-Yan Wang, Jun-Fang Wang, Qun Wang, Ping Yu, Ming-Yi Bai and Min Fan
    J Integr Plant Biol 2020, 62 (4): 421-432.  
    DOI: 10.1111/jipb.12818
    Abstract (Browse 502)  |   Save

    The formation of lateral branches has an important and fundamental contribution to the remarkable developmental plasticity of plants, which allows plants to alter their architecture to adapt to the challenging environment conditions. The Gibberellin (GA) phytohormones have been known to regulate the outgrowth of axillary meristems (AMs), but the specific molecular mechanisms remain unclear. Here we show that DELLA proteins regulate axillary bud formation by interacting and regulating the DNA‐binding ability of SQUAMOSA‐PROMOTER BINDING PROTEIN LIKE 9 (SPL9), a microRNA156‐targeted squamosa promoter binding protein‐like transcription factor. SPL9 participates in the initial regulation of axillary buds by repressing the expression of LATERAL SUPPRESSOR (LAS), a key regulator in the initiation of AMs, and LAS contributes to the specific expression pattern of the GA deactivation enzyme GA2ox4, which is specifically expressed in the axils of leaves to form a low‐GA cell niche in this anatomical region. Nevertheless, increasing GA levels in leaf axils by ectopically expressing the GA‐biosynthesis enzyme GA20ox2 significantly impaired axillary meristem initiation. Our study demonstrates that DELLA‐SPL9‐LAS‐GA2ox4 defines a core feedback regulatory module that spatially pattern GA content in the leaf axil and precisely control the axillary bud formation in different spatial and temporal.

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    Determination of sex by jasmonate
    Claus Wasternack
    J Integr Plant Biol 2020, 62 (2): 162-164.  
    doi: 10.1111/jipb.12840
    Abstract (Browse 334)  |   Save

    Jasmonic acid (JA) and some of its derivatives are important signals in plant stress responses such as biotic or abiotic stresses during alteration of the environment and are signals in several developmental processes such as trichome development, growth/defense balance, root growth, senescence, or light signaling (Wasternack and Hause 2013). Several specific roles of JA are known for proper organ development of flowers. The most prominent example was found by identification of the JA insensitive mutant of Arabidopsis, CORONATINE INSENSITIVE1 (coi1) which is mutated in the F‐Box protein COI1, a component of the JA receptor complex, the Skp1/Cullin/F‐box (SCF) complex. The mutant coi1 is JA‐insensitive and male sterile (cf. rev. Wasternack and Hause 2013). Surprisingly, the corresponding counterpart jai1 of tomato is also JA‐insensitive and altered in the F‐box protein, but is female sterile (cf. rev. Wasternack and Hause 2013).

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    Reactive oxygen species regulate auxin levels to mediate adventitious root induction in Arabidopsis hypocotyl cuttings
    Aixia Huang, Yongshun Wang, Yangyang Liu, Guodong Wang and Xiaoping She
    J Integr Plant Biol 2020, 62 (7): 912-926.  
    DOI: 10.1111/jipb.12870
    Abstract (Browse 365)  |   Save

    Adventitious root (AR) formation from leafy stem cuttings is critical for breeding of many forest and horticultural species. In addition to the plant hormone auxin, wound‐induced signaling caused by the cutting excision is also essential for AR initiation. Here we found that reactive oxygen species (ROS) are rapidly generated at the excision site as a wound‐induced signal and propagated throughout the hypocotyl cutting after excision of the Arabidopsis (Arabidopsis thaliana ) primary root. ROS propagation was not observed in the presence of an NADPH oxidase inhibitor (diphenylene iodonium chloride) or in a knockout mutant of the NADPH oxidase gene respiratory burst oxidase homolog protein D (RBOHD ). Respiratory burst oxidase homolog protein D was specifically upregulated in hypocotyl cuttings at 0.5 h post excision (hpe). Together, these data suggest that RBOHD mediates ROS propagation in hypocotyl cuttings. We also found that auxin levels increased significantly in the shoot apex at 5 hpe and at the base of the cutting at 6 hpe; these effects were blocked by treatment with ROS scavengers. Consistent with this, transcript levels of auxin biosynthesis and polar‐transport genes generally increased between 1 to 6 hpe. Collectively, our results suggest that wound‐induced ROS participate in AR induction through regulation of auxin biosynthesis and transport.

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    Abscisic acid dynamics, signaling, and functions in plants
    Kong Chen, Guo-Jun Li, Ray A. Bressan, Chun-Peng Song, Jian-Kang Zhu and Yang Zhao
    J Integr Plant Biol 2020, 62 (1): 25-54.  
    doi: 10.1111/jipb.12899
    Abstract (Browse 1858)  |   Save

    Abscisic acid (ABA) is an important phytohormone regulating plant growth, development, and stress responses. It has an essential role in multiple physiological processes of plants, such as stomatal closure, cuticular wax accumulation, leaf senescence, bud dormancy, seed germination, osmotic regulation, and growth inhibition among many others. Abscisic acid controls downstream responses to abiotic and biotic environmental changes through both transcriptional and posttranscriptional mechanisms. During the past 20 years, ABA biosynthesis and many of its signaling pathways have been well characterized. Here we review the dynamics of ABA metabolic pools and signaling that affects many of its physiological functions.

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    Colonization of endophyte Acremonium sp. D212 in Panax notoginseng and rice mediated by auxin and jasmonic acid
    Li Han, Xuan Zhou, Yiting Zhao, Shusheng Zhu, Lixia Wu, Yunlu He, Xiangrui Ping, Xinqi Lu, Wuying Huang, Jie Qian, Lina Zhang, Xi Jiang, Dan Zhu, Chongyu Luo, Saijie Li, Qian Dong, Qijing Fu, Kaiyuan Deng, Xin Wang, Lei Wang, Sheng Peng, Jinsong Wu, Weimin Li, Jiří Friml, Youyong Zhu, Xiahong He and Yunlong Du
    J Integr Plant Biol 2020, 62 (9): 1433-1451.  
    DOI: 10.1111/jipb.12905
    Abstract (Browse 369)  |   Save

    Endophytic fungi can be beneficial to plant growth. However, the molecular mechanisms underlying colonization of Acremonium spp. remain unclear. In this study, a novel endophytic Acremonium strain was isolated from the buds of Panax notoginseng and named Acremonium sp. D212. The Acremonium sp. D212 could colonize the roots of P. notoginseng, enhance the resistance of P. notoginseng to root rot disease, and promote root growth and saponin biosynthesis in P. notoginseng. Acremonium sp. D212 could secrete indole‐3‐acetic acid (IAA) and jasmonic acid (JA), and inoculation with the fungus increased the endogenous levels of IAA and JA in P. notoginseng. Colonization of the Acremonium sp. D212 in the roots of the rice line Nipponbare was dependent on the concentration of methyl jasmonate (MeJA) (2–15 μmol/L) and 1‐naphthalenacetic acid (NAA) (10–20 μmol/L). Moreover, the roots of the JA signaling‐defective coi1‐18 mutant were colonized by Acremonium sp. D212 to a lesser degree than those of the wild‐type Nipponbare and miR393b‐overexpressing lines, and the colonization was rescued by MeJA but not by NAA. It suggests that the cross‐talk between JA signaling and the auxin biosynthetic pathway plays a crucial role in the colonization of Acremonium sp. D212 in host plants.

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    Oryza sativa mediator subunit OsMED25 interacts with OsBZR1 to regulate brassinosteroid signaling and plant architecture in rice
    Yuekun Ren, Xiaojie Tian, Shuyu Li, Enyang Mei, Mingliang He, Jiaqi Tang, Min Xu, Xiufeng Li, Zhenyu Wang, Chuanyou Li and Qingyun Bu
    J Integr Plant Biol 2020, 62 (6): 793-811.  
    DOI: 10.1111/jipb.12914
    Abstract (Browse 481)  |   Save

    Brassinosteroids (BRs) are plant‐specific steroid hormones which regulate plant growth, development, and adaptation. Transcriptional regulation plays key roles in plant hormone signaling. A mediator can serve as a bridge between gene‐specific transcription factors and the RNA polymerase machinery, functioning as an essential component in regulating the transcriptional process. However, whether a mediator is involved in BR signaling is unknown. Here, we discovered that Oryza sativa mediator subunit 25 (OsMED25) is an important regulator of rice BR signaling. Phenotypic analyses showed that the OsMED25‐RNAi and osmed25 mutant presented erect leaves, as observed in BR‐deficient mutants. In addition, the OsMED25‐RNAi and osmed25 mutant exhibited decreased BR sensitivity. Genetic analysis indicated that OsMED25‐RNAi could suppress the enhanced BR signaling phenotype of Osbzr1‐D . Further biochemical analysis showed that OsMED25 interacts with OsBZR1 in vivo , and OsMED25 is enriched on the promoter of OsBZR1 target genes. RNA sequencing analysis indicated that OsMED25 affects the expression of approximately 45% of OsBZR1‐regulated genes and mainly functions as a corepressor of OsBZR1. Together, these findings revealed that OsMED25 regulates rice BR signaling by interacting with OsBZR1 and modulating the expression of OsBZR1 target genes, thus expanding our understanding of the roles of mediators in plant hormone signaling.

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    Combined genome‐wide association study and transcriptome analysis reveal candidate genes for resistance to Fusarium ear rot in maize
    Lishan Yao, Yanmei Li, Chuanyu Ma, Lixiu Tong, Feili Du and Mingliang Xu
    J Integr Plant Biol 2020, 62 (10): 1535-1551.  
    doi: 10.1111/jipb.12911
    Abstract (Browse 628)  |   Save

    Fusarium ear rot, caused by Fusarium verticillioides, is a devastating fungal disease in maize that reduces yield and quality; moreover, F. verticillioides produces fumonisin mycotoxins, which pose serious threats to human and animal health. Here, we performed a genome‐wide association study (GWAS) under three environmental conditions and identified 34 single‐nucleotide polymorphisms (SNPs) that were significantly associated with Fusarium ear rot resistance. With reference to the maize B73 genome, 69 genes that overlapped with or were adjacent to the significant SNPs were identified as potential resistance genes to Fusarium ear rot. Comparing transcriptomes of the most resistant and most susceptible lines during the very early response to Fusarium ear rot, we detected many differentially expressed genes enriched for pathways related to plant immune responses, such as plant hormone signal transduction, phenylpropanoid biosynthesis, and cytochrome P450 metabolism. More than one‐fourth of the potential resistance genes detected in the GWAS were differentially expressed in the transcriptome analysis, which allowed us to predict numbers of candidate genes for maize resistance to ear rot, including genes related to plant hormones, a MAP kinase, a PR5‐like receptor kinase, and heat shock proteins. We propose that maize plants initiate early immune responses to Fusarium ear rot mainly by regulating the growth‐defense balance and promoting biosynthesis of defense compounds.

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    Brassinosteroids regulate outer ovule integument growth in part via the control of INNER NO OUTER by BRASSINOZOLE-RESISTANT family transcription factors
    Dandan Jia, Lian-Ge Chen, Guimin Yin, Xiaorui Yang, Zhihua Gao, Yi Guo, Yu Sun and Wenqiang Tang
    J Integr Plant Biol 2020, 62 (8): 1093-1111.  
    doi: 10.1111/jipb.12915
    Abstract (Browse 466)  |   Save

    Brassinosteroids (BRs) play important roles in regulating plant reproductive processes. BR signaling or BR biosynthesis null mutants do not produce seeds under natural conditions, but the molecular mechanism underlying this infertility is poorly understood. In this study, we report that outer integument growth and embryo sac development were impaired in the ovules of the Arabidopsis thaliana BR receptor null mutant bri1‐116 . Gene expression and RNA‐seq analyses showed that the expression of INNER NO OUTER (INO ), an essential regulator of outer integument growth, was significantly reduced in the bri1‐116 mutant. Increased INO expression due to overexpression or increased transcriptional activity of BRASSINAZOLE‐RESISTANT 1 (BZR1) in the mutant alleviated the outer integument growth defect in bri1‐116 ovules, suggesting that BRs regulate outer integument growth partially via BZR1‐mediated transcriptional regulation of INO . Meanwhile, INO expression in bzr‐h , a null mutant for all BZR1 family genes, was barely detectable; and the outer integument of bzr‐h ovules had much more severe growth defects than those of the bri1‐116 mutant. Together, our findings establish a new role for BRs in regulating ovule development and suggest that BZR1 family transcription factors might regulate outer integument growth through both BRI1‐dependent and BRI1‐independent pathways.

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    A bHLH transcription activator regulates defense signaling by nucleo‐cytosolic trafficking in rice
    Fanwei Meng, Chao Yang, Jidong Cao, Huan Chen, Jinhuan Pang, Qiqi Zhao, Zongyi Wang, Zheng Qing Fu and Jun Liu
    J Integr Plant Biol 2020, 62 (10): 1552-1573.  
    doi: 10.1111/jipb.12922
    Abstract (Browse 775)  |   Save

    Crosstalk between plant hormone signaling pathways is vital for controlling the immune response during pathogen invasion. Salicylic acid (SA) and jasmonic acid (JA) often play important but antagonistic roles in the immune responses of higher plants. Here, we identify a basic helix‐loop‐helix transcription activator, OsbHLH6, which confers disease resistance in rice by regulating SA and JA signaling via nucleo‐cytosolic trafficking in rice (Oryza sativa). OsbHLH6 expression was upregulated during Magnaporthe oryzae infection. Transgenic rice plants overexpressing OsbHLH6 display increased JA responsive gene expression and enhanced disease susceptibility to the pathogen. Nucleus‐localized OsbHLH6 activates JA signaling and suppresses SA signaling; however, the SA regulator OsNPR1 (Nonexpressor of PR genes 1) sequesters OsbHLH6 in the cytosol to alleviate its effect. Our data suggest that OsbHLH6 controls disease resistance by dynamically regulating SA and JA signaling.

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    Phytohormone dynamics in developing endosperm influence rice grain shape and quality
    Xiao-Fan Zhang, Jian-Hua Tong, Ai-Ning Bai, Chun-Ming Liu, Lang-Tao Xiao and Hong-Wei Xue
    J Integr Plant Biol 2020, 62 (10): 1625-1637.  
    DOI: 10.1111/jipb.12927
    Abstract (Browse 420)  |   Save

    Hormones are important signaling molecules regulating developmental processes and responses to environmental stimuli in higher plants. Rice endosperm, the portion of the seed surrounding the embryo, is the main determinant of rice grain shape and yield; however, the dynamics and exact functions of phytohormones in developing endosperm remain elusive. Through a systemic study including transcriptome analysis, hormone measurement, and transgene‐based endosperm‐specific expression of phytohormone biosynthetic enzymes, we demonstrated that dynamic phytohormone levels play crucial roles in the developing rice endosperm, particularly in regard to grain shape and quality. We detected diverse, differential, and dramatically changing expression patterns of genes related to hormone biosynthesis and signaling during endosperm development, especially at early developmental stages. Liquid chromatography measurements confirmed the dynamic accumulation of hormones in developing endosperm. Further transgenic analysis performed on plants expressing hormone biosynthesis genes driven by an endosperm‐specific promoter revealed differential effects of the hormones, especially auxin and brassinosteroids, in regulating grain shape and quality. Our studies help elucidate the distinct roles of hormones in developing endosperm and provide novel and useful tools for influencing crop seed shape and yield.

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    Asymmetric cytokinin signaling opposes gravitropism in roots
    Sascha Waidmann and Jürgen Kleine-Vehn
    J Integr Plant Biol 2020, 62 (7): 882-886.  
    doi: 10.1111/jipb.12929
    Abstract (Browse 216)  |   Save

    Plants depend on gravity to provide the constant landmark for downward root growth and upward shoot growth. The phytohormone auxin and its cell‐to‐cell transport machinery are central determinants ensuring gravitropic growth. Statolith sedimentation toward gravity is sensed in specialized cells. This positional cue is translated into the polar distribution of PIN auxin efflux carriers at the plasma membrane, leading to asymmetric auxin distribution and consequently, differential growth and organ bending. While we have started to understand the general principles of how primary organs execute gravitropism, we currently lack basic understanding of how lateral plant organs can defy gravitropic responses. Here we briefly review the establishment of the oblique gravitropic set point angle in lateral roots and particularly discuss the emerging role of asymmetric cytokinin signaling as a central anti‐gravitropic signal. Differential cytokinin signaling is co‐opted in gravitropic lateral and hydrotropic primary roots to counterbalance gravitropic root growth.

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    SmMYB2 promotes salvianolic acid biosynthesis in the medicinal herb Salvia miltiorrhiza
    Changping Deng, Yao Wang, Fenfen Huang, Sunjie Lu, Limei Zhao, Xingyuan Ma and Guoyin Kai
    J Integr Plant Biol 2020, 62 (11): 1688-1702.  
    DOI: 10.1111/jipb.12943
    Abstract (Browse 375)  |   Save

    MYB transcription factors play vital roles in plant growth and metabolism. The phytohormone methyl jasmonate (MeJA) promotes phenolic acid accumulation in the medicinal herb Salvia miltiorrhiza, but the regulatory mechanism is poorly understood. Here, we identified the MeJA‐responsive R2R3‐MYB transcription factor gene SmMYB2 from a transcriptome library produced from MeJA‐treated S. miltiorrhiza hairy roots. SmMYB2 expression was tightly correlated with the expression of key salvianolic acid biosynthetic genes including CYP98A14. SmMYB2 was highly expressed in the periderm of S. miltiorrhiza and SmMYB2 localized to the nucleus. Overexpressing SmMYB2 in S. miltiorrhiza hairy roots significantly increased the levels of salvianolic acids (including rosmarinic acid and salvianolic acid B) by upregulating salvianolic acid biosynthetic genes such as CYP98A14. SmMYB2 binds to the MYB‐binding motifs in the promoter of CYP98A14, as confirmed by a dual‐luciferase assay and electrophoretic mobility shift assays. Anthocyanin contents were significantly higher in SmMYB2‐overexpressing hairy root lines than the control, primarily due to the increased expression of CHI, DFR, and ANS. These findings reveal the novel regulatory role of SmMYB2 in MeJA‐mediated phenolic acid biosynthesis, providing a useful target gene for metabolic engineering and shedding light on the salvianolic acid regulatory network.

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    SlSTE1 promotes abscisic acid‐dependent salt stress‐responsive pathways via improving ion homeostasis and reactive oxygen species scavenging in tomato
    Xiaoqing Meng, Jing Cai, Lei Deng, Ge Li, Jian Sun, Yonghua Han, Tingting Dong, Yang Liu, Tao Xu, Siyuan Liu, Zongyun Li and Mingku Zhu
    J Integr Plant Biol 2020, 62 (12): 1942-1966.  
    DOI: 10.1111/jipb.12987
    Abstract (Browse 313)  |   Save

    High salinity is one of the major limiting factors that reduces crop productivity and quality. Herein, we report that small SALT TOLERANCE ENHANCER1 (STE1) protein without any known conserved domains is required for tomato salt tolerance. Overexpression (OE) of SlSTE1 enhanced the tolerance to multiple chloride salts (NaCl, KCl, and LiCl) and oxidative stress, along with elevated antioxidant enzyme activities, increased abscisic acid (ABA) and chlorophyll contents, and reduced malondialdehyde (MDA) and reactive oxygen species (ROS) accumulations compared to that of wild‐type (WT) plants. Moreover, decreased K+ efflux and increased H+ efflux were detected in the OE plants, which induced a higher K+/Na+ ratio. In contrast, SlSTE1‐RNAi plants displayed decreased tolerance to salt stress. RNA‐seq data revealed 1 330 differentially expressed genes in the OE plants versus WT plants under salt stress, and the transcription of numerous and diverse genes encoding transcription factors, stress‐related proteins, secondary metabolisms, kinases, and hormone synthesis/signaling‐related proteins (notably ABA and 1‐aminocyclopropane‐1‐carboxylate) was greatly elevated. Furthermore, SlSTE1‐OE plants showed increased sensitivity to ABA, and the results suggest that SlSTE1 promotes ABA‐dependent salt stress‐responsive pathways by interacting with SlPYLs and SlSnRK2s. Collectively, our findings reveal that the small SlSTE1 protein confers salt tolerance via ABA signaling and ROS scavenging and improves ion homeostasis in tomato.

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    Integrated metabolo‐transcriptomics and functional characterization reveals that the wheat auxin receptor TIR1 negatively regulates defense against Fusarium graminearum
    Peisen Su, Lanfei Zhao, Wen Li, Jinxiao Zhao, Jun Yan, Xin Ma, Anfei Li, Hongwei Wang and Lingrang Kong
    J Integr Plant Biol 2021, 63 (2): 340-352.  
    doi: 10.1111/jipb.12992
    Abstract (Browse 439)  |   Save
    Fusarium head blight (FHB) caused by Fusarium graminearum Schwabe (teleomorph Gibberella zeae (Schw.) Perch) results in large yield losses in annual global wheat production. Although studies have identified a number of wheat FHB resistance genes, a deeper understanding of the mechanisms underlying host plant resistance to F. graminearum is required for the control of FHB. Here, an integrated metabolomics and transcriptomics analysis of infected wheat plants (Triticum aestivum L.) enabled identification of 789 differentially accumulated metabolites, including flavonoids, phenolamides, tryptamine derivatives, and phytohormones, and revealed altered expression of more than 100 genes that function in the biosynthesis or regulation of these pathways. Our data regarding the effects of F. graminearum infection on flavonoids and auxin signaling led to follow‐up experiments that showed that exogenous kaempferide and apigenin application on spikes increased wheat resistance to FHB, while exogenous auxin treatment increased FHB susceptibility. RNAi‐mediated knockdown of the gene encoding the auxin receptor, TaTIR1, increased FHB resistance. Our data supported the use of TaTIR1 knockdown in controlling FHB. Our study provides insights on the wheat response to F. graminearum infection and its FHB resistance mechanisms while illustrating the potential of TaTIR1 knockdown in increasing FHB resistance during crop improvement programs.
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    Function identification of MdTIR1 in apple root growth benefited from the predicted MdPPI network
    Lin Liu, Zipeng Yu, Yang Xu, Cheng Guo, Lei Zhang, Changai Wu, Guodong Yang, Jinguang Huang, Kang Yan, Huairui Shu, Chengchao Zheng and Shizhong Zhang
    J Integr Plant Biol 2021, 63 (4): 723-739.  
    DOI: 10.1111/jipb.12996
    Abstract (Browse 280)  |   Save
    Protein–protein interaction (PPI) network analysis is an effective method to identify key proteins during plant development, especially in species for which basic molecular research is lacking, such as apple (Malus domestica). Here, an MdPPI network containing 30 806 PPIs was inferred in apple and its quality and reliability were rigorously verified. Subsequently, a root‐growth subnetwork was extracted to screen for critical proteins in root growth. Because hormone‐related proteins occupied the largest proportion of critical proteins, a hormone‐related sub‐subnetwork was further extracted from the root‐growth subnetwork. Among these proteins, auxin‐related M. domestica TRANSPORT INHIBITOR RESISTANT 1 (MdTIR1) served as the central, high‐degree node, implying that this protein exerts essential roles in root growth. Furthermore, transgenic apple roots overexpressing an MdTIR1 transgene displayed increased primary root elongation. Expression analysis showed that MdTIR1 significantly upregulated auxin‐responsive genes in apple roots, indicating that it mediates root growth in an auxin‐dependent manner. Further experimental validation revealed that MdTIR1 interacted with and accelerated the degradation of MdIAA28, MdIAA43, and MdIAA46. Thus, MdTIR1‐mediated degradation of MdIAAs is critical in auxin signal transduction and root growth regulation in apple. Moreover, our network analysis and high‐degree node screening provide a novel research technique for more generally characterizing molecular mechanisms.
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    The role of light in regulating seed dormancy and germination
    Liwen Yang, Shuangrong Liu and Rongcheng Lin
    J Integr Plant Biol 2020, 62 (9): 1310-1326.  
    doi: 10.1111/jipb.13001
    Abstract (Browse 341)  |   Save

    Seed dormancy is an adaptive trait in plants. Breaking seed dormancy determines the timing of germination and is, thereby essential for ensuring plant survival and agricultural production. Seed dormancy and the subsequent germination are controlled by both internal cues (mainly hormones) and environmental signals. In the past few years, the roles of plant hormones in regulating seed dormancy and germination have been uncovered. However, we are only beginning to understand how light signaling pathways modulate seed dormancy and interaction with endogenous hormones. In this review, we summarize current views of the molecular mechanisms by which light controls the induction, maintenance and release of seed dormancy, as well as seed germination, by regulating hormone metabolism and signaling pathways.

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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 419)  |   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 pre‐mRNA splicing factor RDM16 regulates root stem cell maintenance in Arabidopsis
    Bingsheng Lv, Kongqin Hu, Te Tian, Kaijing Wei, Feng Zhang, Yuebin Jia, Huiyu Tian and Zhaojun Ding
    J Integr Plant Biol 2021, 63 (4): 662-678.  
    DOI: 10.1111/jipb.13006
    Abstract (Browse 424)  |   Save
    Pre‐mRNA (messenger RNA) splicing participates in the regulation of numerous biological processes in plants. For example, alternative splicing shapes transcriptomic responses to abiotic and biotic stress, and controls developmental programs. However, no study has revealed a role for splicing in maintaining the root stem cell niche. Here, a screen for defects in root growth in Arabidopsis thaliana identified an ethyl methane sulfonate mutant defective in pre‐mRNA splicing (rdm16‐4). The rdm16‐4 mutant displays a short‐root phenotype resulting from fewer cells in the root apical meristem. The PLETHORA1 (PLT1) and PLT2 transcription factor genes are important for root development and were alternatively spliced in rdm16‐4 mutants, resulting in a disordered root stem cell niche and retarded root growth. The root cap of rdm16‐4 contained reduced levels of cytokinins, which promote differentiation in the developing root. This reduction was associated with the alternative splicing of genes encoding cytokinin signaling factors, such as ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN5 and ARABIDOPSIS RESPONSE REGULATORS (ARR1, ARR2, and ARR11). Furthermore, expression of the full‐length coding sequence of ARR1 or exogenous cytokinin application partially rescued the short‐root phenotype of rdm16‐4. This reveals that the RDM16‐mediated alternative splicing of cytokinin signaling components contributes to root growth.
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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 296)  |   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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    Suppression of DRR1 results in the accumulation of insoluble ubiquitinated proteins, which impairs drought stress tolerance
    Seong Gwan Yu, Na Hyun Cho, Jong Hum Kim, Tae Rin Oh and Woo Taek Kim
    J Integr Plant Biol 2021, 63 (3): 431-437.  
    doi: 10.1111/jipb.13014
    Abstract (Browse 820)  |   Save
    Drought stress has detrimental effects on plants. Although the abscisic acid (ABA)‐mediated drought response is well established, defensive mechanisms to cope with dehydration‐induced proteotoxicity have been rarely studied. DRR1 was identified as an Arabidopsis drought‐induced gene encoding an ER‐localized RING‐type E3 Ub ligase. Suppression of DRR1 markedly reduced tolerance to drought and proteotoxic stress without altering ABA‐mediated germination and stomatal movement. Proteotoxicity‐ and dehydration‐induced insoluble ubiquitinated protein accumulation was more obvious in DRR1 loss‐of‐function plants than in wild‐type plants. These results suggest that DRR1 is involved in an ABA‐independent drought stress response possibly through the mitigation of dehydration‐induced proteotoxic stress.
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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 433)  |   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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    Comparative transcriptomics reveals hidden issues in the plant response to arthropod herbivores
    M. Estrella Santamaria, Alejandro Garcia, Ana Arnaiz, Irene Rosa‐Diaz, Gara Romero‐Hernandez, IsabelDiaz and Manuel Martinez
    J Integr Plant Biol 2021, 63 (2): 312-326.  
    doi: 10.1111/jipb.13026
    Abstract (Browse 304)  |   Save
    Plants experience different abiotic/biotic stresses, which trigger their molecular machinery to cope with them. Besides general mechanisms prompted by many stresses, specific mechanisms have been introduced to optimize the response to individual threats. However, these key mechanisms are difficult to identify. Here, we introduce an in‐depth species‐specific transcriptomic analysis and conduct an extensive meta‐analysis of the responses to related species to gain more knowledge about plant responses. The spider mite Tetranychus urticae was used as the individual species, several arthropod herbivores as the related species for meta‐analysis, and Arabidopsis thaliana plants as the common host. The analysis of the transcriptomic data showed typical common responses to herbivory, such as jasmonate signaling or glucosinolate biosynthesis. Also, a specific set of genes likely involved in the particularities of the Arabidopsis‐spider mite interaction was discovered. The new findings have determined a prominent role in this interaction of the jasmonate‐induced pathways leading to the biosynthesis of anthocyanins and tocopherols. Therefore, tandem individual/general transcriptomic profiling has been revealed as an effective method to identify novel relevant processes and specificities in the plant response to environmental stresses.
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    Ethylene signaling in rice and Arabidopsis: New regulators and mechanisms
    He Zhao, Cui-Cui Yin, Biao Ma, Shou-Yi Chen and Jin-Song Zhang
    J Integr Plant Biol 2021, 63 (1): 102-125.  
    doi: 10.1111/jipb.13028
    Abstract (Browse 449)  |   Save
    Ethylene is a gaseous hormone which plays important roles in both plant growth and development and stress responses. Based on studies in the dicot model plant species Arabidopsis, a linear ethylene signaling pathway has been established, according to which ethylene is perceived by ethylene receptors and transduced through CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) and ETHYLENE‐INSENSITIVE 2 (EIN2) to activate transcriptional reprogramming. In addition to this canonical signaling pathway, an alternative ethylene receptor‐mediated phosphor‐relay pathway has also been proposed to participate in ethylene signaling. In contrast to Arabidopsis, rice, a monocot, grows in semiaquatic environments and has a distinct plant structure. Several novel regulators and/or mechanisms of the rice ethylene signaling pathway have recently been identified, indicating that the ethylene signaling pathway in rice has its own unique features. In this review, we summarize the latest progress and compare the conserved and divergent aspects of the ethylene signaling pathway between Arabidopsis and rice. The crosstalk between ethylene and other plant hormones is also reviewed. Finally, we discuss how ethylene regulates plant growth, stress responses and agronomic traits. These analyses should help expand our knowledge of the ethylene signaling mechanism and could further be applied for agricultural purposes.
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    Light participates in the auxin‐dependent regulation of plant growth
    Bingsheng Lv, Jiayong Zhu, Xiangpei Kong and Zhaojun Ding
    J Integr Plant Biol 2021, 63 (5): 819-822.  
    doi: 10.1111/jipb.13036
    Abstract (Browse 328)  |   Save
    Light is the energy source for plant photosynthesis and influences plant growth and development. Through multiple photoreceptors, plant interprets light signals through various downstream phytohormones such as auxin. Recently, Chen et al. (2020) uncover a new layer of regulation in IPyA pathway of auxin biosynthesis by light. Here we highlight recent studies about how light controls plant growth through regulating auxin biosynthesis and signaling.
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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 374)  |   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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    The novel peptide NbPPI1 identified from Nicotiana benthamiana triggers immune responses and enhances resistance against Phytophthora pathogens
    Qujiang Wen, Manli Sun, Xianglan Kong, Yang Yang, Qiang Zhang, Guiyan Huang, Wenqin Lu, Wanyue Li, Yuling Meng and Weixing Shan
    J Integr Plant Biol 2021, 63 (5): 961-976.  
    DOI: 10.1111/jipb.13033
    Abstract (Browse 294)  |   Save
    In plants, recognition of small secreted peptides, such as damage/danger‐associated molecular patterns (DAMPs), regulates diverse processes, including stress and immune responses. Here, we identified an SGPS (Ser‐Gly‐Pro‐Ser) motif‐containing peptide, Nicotiana tabacum NtPROPPI, and its two homologs in Nicotiana benthamiana, NbPROPPI1 and NbPROPPI2. Phytophthora parasitica infection and salicylic acid (SA) treatment induced NbPROPPI1/2 expression. Moreover, SignalP predicted that the 89‐amino acid NtPROPPI includes a 24‐amino acid N‐terminal signal peptide and NbPROPPI1/2‐GFP fusion proteins were mainly localized to the periplasm. Transient expression of NbPROPPI1/2 inhibited P. parasitica colonization, and NbPROPPI1/2 knockdown rendered plants more susceptible to P. parasitica. An eight‐amino‐acid segment in the NbPROPPI1 C‐terminus was essential for its immune function and a synthetic 20‐residue peptide, NbPPI1, derived from the C‐terminus of NbPROPPI1 provoked significant immune responses in N. benthamiana. These responses led to enhanced accumulation of reactive oxygen species, activation of mitogen‐activated protein kinases, and up‐regulation of the defense genes Flg22‐induced receptor‐like kinase (FRK) and WRKY DNA‐binding protein 33 (WRKY33). The NbPPI1‐induced defense responses require Brassinosteroid insensitive 1‐associated receptor kinase 1 (BAK1). These results suggest that NbPPI1 functions as a DAMP in N. benthamiana; this novel DAMP provides a potentially useful target for improving plant resistance to Pytophthora pathogens.
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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 271)  |   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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    Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice
    Farhan Ullah, Qiutao Xu, Yu Zhao and Dao‐Xiu Zhou
    J Integr Plant Biol 2021, 63 (3): 451-467.  
    doi: 10.1111/jipb.13042
    Abstract (Browse 651)  |   Save
    Plants have evolved numerous mechanisms that assist them in withstanding environmental stresses. Histone deacetylases (HDACs) play crucial roles in plant stress responses; however, their regulatory mechanisms remain poorly understood. Here, we explored the function of HDA710/OsHDAC2, a member of the HDAC RPD3/HDA1 family, in stress tolerance in rice (Oryza sativa). We established that HDA710 localizes to both the nucleus and cytoplasm and is involved in regulating the acetylation of histone H3 and H4, specifically targeting H4K5 and H4K16 under normal conditions. HDA710 transcript accumulation levels were strongly induced by abiotic stresses including drought and salinity, as well as by the phytohormones jasmonic acid (JA) and abscisic acid (ABA). hda710 knockout mutant plants showed enhanced salinity tolerance and reduced ABA sensitivity, whereas transgenic plants overexpressing HDA710 displayed the opposite phenotypes. Moreover, ABA‐ and salt‐stress‐responsive genes, such as OsLEA3, OsABI5, OsbZIP72, and OsNHX1, were upregulated in hda710 compared with wild‐type plants. These expression differences corresponded with higher levels of histone H4 acetylation in gene promoter regions in hda710 compared with the wild type under ABA and salt‐stress treatment. Collectively, these results suggest that HDA710 is involved in regulating ABA‐ and salt‐stress‐responsive genes by altering H4 acetylation levels in their promoters.
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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 303)  |   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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    Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions
    Nai-Qian Dong and Hong-Xuan Lin
    J Integr Plant Biol 2021, 63 (1): 180-209.  
    doi: 10.1111/jipb.13054
    Abstract (Browse 717)  |   Save
    Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant–environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plant–environment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post‐transcriptional, post‐translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.
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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 536)  |   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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    Mediator tail module subunits MED16 and MED25 differentially regulate abscisic acid signaling in Arabidopsis
    Pengcheng Guo, Leelyn Chong, Fangming Wu, Chuan‐Chih Hsu, Chuanyou Li, Jian‐Kang Zhu and Yingfang Zhu
    J Integr Plant Biol 2021, 63 (4): 802-815.  
    DOI: 10.1111/jipb.13062
    Abstract (Browse 318)  |   Save
    MED25 has been implicated as a negative regulator of the abscisic acid (ABA) signaling pathway. However, it is unclear whether other Mediator subunits could associate with MED25 to participate in the ABA response. Here, we used affinity purification followed by mass spectrometry to uncover Mediator subunits that associate with MED25 in transgenic plants. We found that at least 26 Mediator subunits, belonging to the head, middle, tail, and CDK8 kinase modules, were co‐purified with MED25 in vivo. Interestingly, the tail module subunit MED16 was identified to associate with MED25 under both mock and ABA treatments. We further showed that the disruption of MED16 led to reduced ABA sensitivity compared to the wild type. Transcriptomic analysis revealed that the expression of several ABA‐responsive genes was significantly lower in med16 than those in wild type. Furthermore, we discovered that MED16 may possibly compete with MED25 to interact with the key transcription factor ABA INSENSITIVE 5 (ABI5) to positively regulate ABA signaling. Consistently, med16 and med25 mutants displayed opposite phenotypes in ABA response, cuticle permeability, and differential ABI5‐mediated EM1 and EM6 expression. Together, our data indicate that MED16 and MED25 differentially regulate ABA signaling by antagonistically affecting ABI5‐mediated transcription in Arabidopsis.
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    Arabidopsis U‐box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor‐like protein kinases LRR1 and KIN7
    Xuexue Chen, Tingting Wang, Amin Ur Rehman, Yu Wang, Junsheng Qi, Zhen Li, Chunpeng Song, Baoshan Wang, Shuhua Yang and Zhizhong Gong
    J Integr Plant Biol 2021, 63 (3): 494-509.  
    doi: 10.1111/jipb.13058
    Abstract (Browse 690)  |   Save
    Both plant receptor‐like protein kinases (RLKs) and ubiquitin‐mediated proteolysis play crucial roles in plant responses to drought stress. However, the mechanism by which E3 ubiquitin ligases modulate RLKs is poorly understood. In this study, we showed that Arabidopsis PLANT U‐BOX PROTEIN 11 (PUB11), an E3 ubiquitin ligase, negatively regulates abscisic acid (ABA)‐mediated drought responses. PUB11 interacts with and ubiquitinates two receptor‐like protein kinases, LEUCINE RICH REPEAT PROTEIN 1 (LRR1) and KINASE 7 (KIN7), and mediates their degradation during plant responses to drought stress in vitro and in vivo. pub11 mutants were more tolerant, whereas lrr1 and kin7 mutants were more sensitive, to drought stress than the wild type. Genetic analyses show that the pub11 lrr1 kin7 triple mutant exhibited similar drought sensitivity as the lrr1 kin7 double mutant, placing PUB11 upstream of the two RLKs. Abscisic acid and drought treatment promoted the accumulation of PUB11, which likely accelerates LRR1 and KIN7 degradation. Together, our results reveal that PUB11 negatively regulates plant responses to drought stress by destabilizing the LRR1 and KIN7 RLKs.
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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 311)  |   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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    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 440)  |   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 454)  |   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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    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 334)  |   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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    Protein farnesylation negatively regulates brassinosteroid signaling via reducing BES1 stability in Arabidopsis thaliana
    Zengxiu Feng, Hongyong Shi, Minghui Lv, Yuang Ma and Jia Li
    J Integr Plant Biol 2021, 63 (7): 1353-1366.  
    doi: 10.1111/jipb.13093
    Abstract (Browse 294)  |   Save
    Brassinosteroids (BRs) are a group of steroidal phytohormones, playing critical roles in almost all physiological aspects during the life span of a plant. In Arabidopsis, BRs are perceived at the cell surface, triggering a reversible phosphorylation-based signaling cascade that leads to the activation and nuclear accumulation of a family of transcription factors, represented by BES1 and BZR1. Protein farnesylation is a type of post-translational modification, functioning in many important cellular processes. Previous studies demonstrated a role of farnesylation in BR biosynthesis via regulating the endoplasmic reticulum localization of a key bassinolide (BL) biosynthetic enzyme BR6ox2. Whether such a process is also involved in BR signaling is not understood. Here, we demonstrate that protein farnesylation is involved in mediating BR signaling in Arabidopsis. A loss-of-function mutant of ENHANCED RESPONSE TO ABA 1 (ERA1), encoding a β subunit of the protein farnesyl transferase holoenzyme, can alter the BL sensitivity of bak1-4 from a reduced to a hypersensitive level. era1 can partially rescue the BR defective phenotype of a heterozygous mutant of bin2-1, a gain-of-function mutant of BIN2 which encodes a negative regulator in the BR signaling. Our genetic and biochemical analyses revealed that ERA1 plays a significant role in regulating the protein stability of BES1.
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