Root development

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    A member of the ALOG gene family has a novel role in regulating nodulation in Lotus japonicus
    Yawen Lei, Shihao Su, Liang He, Xiaohe Hu and Da Luo
    J Integr Plant Biol 2019, 61 (4): 463-477.  
    doi: 10.1111/jipb.12711
    Abstract (Browse 1043)  |   Save

    Legumes can control the number of symbiotic nodules that form on their roots, thus balancing nitrogen assimilation and energy consumption. Two major pathways participate in nodulation: the Nod factor (NF) signaling pathway which involves recognition of rhizobial bacteria by root cells and promotion of nodulation, and the autoregulation of nodulation (AON) pathway which involves long-distance negative feedback between roots and shoots. Although a handful of genes have a clear role in the maintenance of nodule number, additional unknown factors may also be involved in this process. Here, we identify a novel function for a Lotus japonicus ALOG (Arabidopsis LSH1 and Oryza G1) family member, LjALOG1, involved in positively regulating nodulation. LjALOG1 expression increased substantially after inoculation with rhizobia, with high levels of expression in whole nodule primordia and in the base of developing nodules. The ljalog1 mutants, which have an insertion of the LORE1 retroelement in LjALOG1, had significantly fewer nodules compared with wild type, along with increased expression of LjCLE-RS1 (L. japonicus CLE Root Signal 1), which encodes a nodulation suppressor in the AON pathway. In summary, our findings identified a novel factor that participates in controlling nodulation, possibly by suppressing the AON pathway.

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    Rhizosheath formation and involvement in foxtail millet (Setaria italica) root growth under drought stress
    Tie-Yuan Liu, Nenghui Ye, Tao Song, Yunying Cao, Bei Gao, Di Zhang, Fuyuan Zhu, Moxian Chen, Yingjiao Zhang, Weifeng Xu and Jianhua Zhang
    J Integr Plant Biol 2019, 61 (4): 449-462.  
    DOI: 10.1111/jipb.12716
    Abstract (Browse 296)  |   Save
    The rhizosheath, a layer of soil particles that adheres firmly to the root surface by a combination of root hairs and mucilage, may improve tolerance to drought stress. Setaria italica (L.) P. Beauv. (foxtail millet), a member of the Poaceae family, is an important food and fodder crop in arid regions and forms a larger rhizosheath under drought conditions. Rhizosheath formation under drought conditions has been studied, but the regulation of root hair growth and rhizosheath size in response to soil moisture remains unclear. To address this question, in this study we monitored root hair growth and rhizosheath development in response to a gradual decline in soil moisture. Here, we determined that a soil moisture level of 10%–14% (w/w) stimulated greater rhizosheath production compared to other soil moisture levels. Root hair density and length also increased at this soil moisture level, which was validated by measurement of the expression of root hair-related genes. These findings contribute to our understanding of rhizosheath formation in response to soil water stress.
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    REF6 promotes lateral root formation through de-repression of PIN1/3/7 genes
    Xiaolei Wang, Jiong Gao, Shan Gao, Zhongpeng Li, Benke Kuai and Guodong Ren
    J Integr Plant Biol 2019, 61 (4): 383-387.  
    doi: 10.1111/jipb.12726
    Abstract (Browse 274)  |   Save
    The H3K27 methyltransferase CLF inhibits lateral root (LR) formation through depositing the repressive H3K27me3 mark to the chromatin of PIN1, a key polar auxin transporter gene. Here, we show that the H3K27me3 demethylase REF6 promotes lateral root primordium initiation and LR emergence. REF6 directly binds to the chromatin of PIN1/3/7. Dysfunction in REF6 results in increased levels of H3K27me3 on PIN1/3/7 and suppressed expression of PIN genes. Genetic analysis of the clf ref6 double mutant revealed an antagonistic action between CLF and REF6, in terms of LR formation. Our findings indicate that H3K27 methylation and demethylation activities are likely coordinated to ensure proper LR organogenesis.
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    The Brassicaceae-specific secreted peptides, STMPs, function in plant growth and pathogen defense
    Zipeng Yu, Yang Xu, Lifei Zhu, Lei Zhang, Lin Liu, Di Zhang, Dandan Li, Changai Wu, Jinguang Huang, Guodong Yang, Kang Yan, Shizhong Zhang and Chengchao Zheng
    J Integr Plant Biol 2020, 62 (4): 403-420.  
    DOI: 10.1111/jipb.12817
    Abstract (Browse 365)  |   Save

    Low molecular weight secreted peptides have recently been shown to affect multiple aspects of plant growth, development, and defense responses. Here, we performed stepwise BLAST filtering to identify unannotated peptides from the Arabidopsis thaliana protein database and uncovered a novel secreted peptide family, secreted transmembrane peptides (STMPs). These low molecular weight peptides, which consist of an N‐terminal signal peptide and a transmembrane domain, were primarily localized to extracellular compartments but were also detected in the endomembrane system of the secretory pathway, including the endoplasmic reticulum and Golgi. Comprehensive bioinformatics analysis identified 10 STMP family members that are specific to the Brassicaceae family. Brassicaceae plants showed dramatically inhibited root growth upon exposure to chemically synthesized STMP1 and STMP2. Arabidopsis overexpressing STMP1, 2, 4, 6, or 10 exhibited severely arrested growth, suggesting that STMPs are involved in regulating plant growth and development. In addition, in vitro bioassays demonstrated that STMP1, STMP2, and STMP10 have antibacterial effects against Pseudomonas syringae pv. tomato DC3000, Ralstonia solanacearum, Bacillus subtilis, and Agrobacterium tumefaciens, demonstrating that STMPs are antimicrobial peptides. These findings suggest that STMP family members play important roles in various developmental events and pathogen defense responses in Brassicaceae plants.

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    Intersected functional zone of transcriptional regulators patterns stemness within stem cell niche of root apical meristem
    Meizhi Xu, Xu Gu, Nengsong Liang, Xinxin Bian, Hong Wang, Yaxin Qin, Limin Pi and Shuang Wu
    J Integr Plant Biol 2020, 62 (7): 897-911.  
    DOI: 10.1111/jipb.12881
    Abstract (Browse 337)  |   Save

    Root stem cell niche (SCN) consists of a quiescent center (QC) and surrounding stem cells. Disrupted symplastic communication leads to loss of stemness in the whole SCN. Several SCN regulators were reported to move between cells for SCN maintenance. However, single mutant of these regulators is insufficient to abolish QC stemness despite the high differentiation rate in surrounding stem cells. To dissect the mechanism behind such distinct stemness in SCN, we combined the mis‐expression strategy with pWOX5:icals3m system in which QC is symplastically isolated. We found the starch accumulation in QC could be synergistically repressed by WUSCHEL‐RELATED HOMEOBOX 5 (WOX5), SHORT‐ROOT (SHR), SCARCROW (SCR), and PLETHORA (PLT). Like PLTs, other core regulators also exhibited dimorphic functions by inhibiting differentiation at a higher dose while promoting cell division at a low protein level. Being located in the center of the intersected expression zones, QC cells receive the highest level of core regulators, forming the most robust stemness within SCN. WUSCHEL‐RELATED HOMEOBOX 5 was sufficient to activate PLT1/2 expression, contributing to the QC‐enriched PLTs. Our results provide experimental evidence supporting the long‐standing hypothesis that the combination of spatial expression, synergistic function and dosage effect of core regulators result in spatially distinct stemness in SCN.

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    The interaction of CaM7 and CNGC14 regulates root hair growth in Arabidopsis
    Qudsia Zeb, Xiaohan Wang, Congcong Hou, Xiwen Zhang, Mengqi Dong, Sisi Zhang, Qian Zhang, Zhijie Ren, Wang Tian, Huifen Zhu, Legong Li and Liangyu Liu
    J Integr Plant Biol 2020, 62 (7): 887-896.  
    DOI: 10.1111/jipb.12890
    Abstract (Browse 472)  |   Save

    Oscillations in cytosolic free calcium determine the polarity of tip‐growing root hairs. The Ca2+ channel cyclic nucleotide gated channel 14 (CNGC14) contributes to the dynamic changes in Ca2+ concentration gradient at the root hair tip. However, the mechanisms that regulate CNGC14 are unknown. In this study, we detected a direct interaction between calmodulin 7 (CaM7) and CNGC14 through yeast two‐hybrid and bimolecular fluorescence complementation assays. We demonstrated that the third EF‐hand domain of CaM7 specifically interacts with the cytosolic C‐terminal domain of CNGC14. A two‐electrode voltage clamp assay showed that CaM7 completely inhibits CNGC14‐mediated Ca2+ influx, suggesting that CaM7 negatively regulates CNGC14‐mediated calcium signaling. Furthermore, CaM7 overexpressing lines phenocopy the short root hair phenotype of a cngc14 mutant and this phenotype is insensitive to changes in external Ca2+ concentrations. We, thus, identified CaM7‐CNGC14 as a novel interacting module that regulates polar growth in root hairs by controlling the tip‐focused Ca2+ signal.

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    Aluminium is essential for root growth and development of tea plants (Camellia sinensis )
    Lili Sun, Mengshi Zhang, Xiaomei Liu, Qianzhuo Mao, Chen Shi, Leon V. Kochian and Hong Liao
    J Integr Plant Biol 2020, 62 (7): 984-997.  
    doi: 10.1111/jipb.12942
    Abstract (Browse 603)  |   Save

    On acid soils, the trivalent aluminium ion (Al3+) predominates and is very rhizotoxic to most plant species. For some native plant species adapted to acid soils including tea (Camellia sinensis ), Al3+ has been regarded as a beneficial mineral element. In this study, we discovered that Al3+ is actually essential for tea root growth and development in all the tested varieties. Aluminum ion promoted new root growth in five representative tea varieties with dose‐dependent responses to Al3+ availability. In the absence of Al3+, the tea plants failed to generate new roots, and the root tips were damaged within 1 d of Al deprivation. Structural analysis of root tips demonstrated that Al was required for root meristem development and activity. In situ morin staining of Al3+ in roots revealed that Al mainly localized to nuclei in root meristem cells, but then gradually moved to the cytosol when Al3+ was subsequently withdrawn. This movement of Al3+ from nuclei to cytosols was accompanied by exacerbated DNA damage, which suggests that the nuclear‐targeted Al primarily acts to maintain DNA integrity. Taken together, these results provide novel evidence that Al3+ is essential for root growth in tea plants through maintenance of DNA integrity in meristematic cells.

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    SHY2 as a node in the regulation of root meristem development by auxin, brassinosteroids, and cytokinin
    Taotao Li, Xinke Kang, Wei Lei, Xiuhong Yao, Lijuan Zou, Dawei Zhang and Honghui Lin
    J Integr Plant Biol 2020, 62 (10): 1500-1517.  
    DOI: 10.1111/jipb.12931
    Abstract (Browse 342)  |   Save
    In multicellular organisms, the balance between cell division and differentiation determines organ size, and represents a central unknown in developmental biology. In Arabidopsis roots, this balance is mediated between cytokinin and auxin through a regulatory circuit converging on the IAA3/SHORT HYPOCOTYL 2 (SHY2) gene. Here, we show that crosstalk between brassinosteroids (BRs) and auxin occurs in the vascular transition zone to promote root meristem development. We found that BR increases root meristem size by up‐regulating expression of the PINFORMED 7 (PIN7) gene and down‐regulating expression of the SHY2 gene. In addition, BES1 could directly bind to the promoter regions of both PIN7 and SHY2, indicating that PIN7 and SHY2 mediate the BR‐induced growth of the root meristem by serving as direct targets of BES1. Moreover, the PIN7 overexpression and loss‐of‐function SHY2 mutant were sensitive to the effects of BR and could partially suppress the short‐root phenotypes associated with deficient BR signaling. Interestingly, BRs could inhibit the accumulation of SHY2 protein in response to cytokinin. Taken together, these findings suggest that a complex equilibrium model exists in which regulatory interactions among BRs, auxin, and cytokinin regulate optimal root growth.
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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 425)  |   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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    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 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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    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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    SIZ1 negatively regulates aluminum resistance by mediating the STOP1–ALMT1 pathway in Arabidopsis
    Jiameng Xu, Jiayong Zhu, Jiajia Liu, Junxia Wang, Zhaojun Ding and Huiyu Tian
    J Integr Plant Biol 2021, 63 (6): 1147-1160.  
    DOI: 10.1111/jipb.13091
    Abstract (Browse 355)  |   Save
    Sensitive to proton rhizotoxicity 1 (STOP1) functions as a crucial regulator of root growth during aluminum (Al) stress. However, how this transcription factor is regulated by Al stress to affect downstream genes expression is not well understood. To explore the underlying mechanisms of the function and regulation of STOP1, we employed a yeast two hybrid screen to identify STOP1-interacting proteins. The SUMO E3 ligase SIZ1, was found to interact with STOP1 and mainly facilitate its SUMO modification at K40 and K212 residues. Simultaneous introduction of K40R and K212R substitutions in STOP1 enhances its transactivation activity to upregulate the expression of aluminum-activated malate transporter 1 (ALMT1) via increasing the association with mediator 16 (MED16) transcriptional co-activator. Loss of function of SIZ1 causes highly increased expression of ALMT1, thus enhancing Al-induced malate exudation and Al tolerance. Also, we found that the protein level of SIZ1 is reduced in response to Al stress. Genetic evidence demonstrates that STOP1/ALMT1 is epistatic to SIZ1 in regulating root growth response to Al stress. This study suggests a mechanism about how the SIZ1–STOP1–ALMT1 signaling module is involved in root growth response to Al stress.
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    HY5 regulates light-responsive transcription of microRNA163 to promote primary root elongation in Arabidopsis seedlings
    Tao Li, Hongmei Lian, Haojie Li, Yufang Xu and Huiyong Zhang
    J Integr Plant Biol 2021, 63 (8): 1437-1450.  
    doi: 10.1111/jipb.13099
    Abstract (Browse 350)  |   Save
    MicroRNAs (miRNAs) play key roles in the post-transcriptional regulation of gene expression in plants. Many miRNAs are responsive to environmental signals. Light is the first environmental signal perceived by plants after emergence from the soil. However, less is known about the roles and regulatory mechanism of miRNAs in response to light signal. Here, using small RNA sequencing, we determined that miR163 is significantly rapidly induced by light signaling in Arabidopsis thaliana seedlings. The light-inducible response of miR163 functions genetically downstream of LONG HYPOCOTYL 5 (HY5), a central positive regulator of photomorphogenesis. HY5 directly binds to the two G/C-hybrid elements in the miR163 promoter with unequal affinity; one of these elements, which is located next to the transcription start site, plays a major role in light-induced expression of miR163. Overexpression of miR163 rescued the defective primary root elongation of hy5 seedlings without affecting lateral root growth, whereas overexpressing of miR163 target PXMT1 inhibited primary root elongation. These findings provide insight into understanding the post-transcriptional regulation of root photomorphogenesis mediated by the HY5-miR163-PXMT1 network.
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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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