Two Leucine-Rich Repeat Receptor Kinases Mediate Signaling, Linking Cell Wall Biosynthesis and ACC Synthase in Arabidopsis

Article (PDF Available)inThe Plant Cell 20(11):3065-79 · December 2008with28 Reads
DOI: 10.1105/tpc.108.063354 · Source: PubMed
Abstract
The plant cell wall is a dynamic structure that changes in response to developmental and environmental cues through poorly understood signaling pathways. We identified two Leu-rich repeat receptor-like kinases in Arabidopsis thaliana that play a role in regulating cell wall function. Mutations in these FEI1 and FEI2 genes (named for the Chinese word for fat) disrupt anisotropic expansion and the synthesis of cell wall polymers and act additively with inhibitors or mutations disrupting cellulose biosynthesis. While FEI1 is an active protein kinase, a kinase-inactive version of FEI1 was able to fully complement the fei1 fei2 mutant. The expansion defect in fei1 fei2 roots was suppressed by inhibition of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase, an enzyme that converts Ado-Met to ACC in ethylene biosynthesis, but not by disruption of the ethylene response pathway. Furthermore, the FEI proteins interact directly with ACC synthase. These results suggest that the FEI proteins define a novel signaling pathway that regulates cell wall function, likely via an ACC-mediated signal.

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    • "Three LRR RLKs were also found in the two QTLs associated with BFS and length (Table 5 , Figures 6 and 7). In Arabidopsis elongating root tips and seeds, two LRR RLKs named FEI 1 and 2 have been reported to play a role in cellulose deposition in Arabidopsis elongating root tips [34] and seed coat [35] . ACC (1-aminocyclopropane-1-carbox- ylic acid) that is essential for ethylene signaling has been suggested to be a signaling molecule for FEI 1 and 2 [58], so both ethylene and LRR RLK signaling are most likely involved in cellulose deposition in elongating tissues (Fig. 8). "
    [Show abstract] [Hide abstract] ABSTRACT: Background Individual fiber strength is an important quality attribute that greatly influences the strength of the yarn spun from cotton fibers. Fiber strength is usually measured from bundles of fibers due to the difficulty of reliably measuring strength from individual cotton fibers. However, bundle fiber strength (BFS) is not always correlated with yarn strength since it is affected by multiple fiber properties involved in fiber-to-fiber interactions within a bundle in addition to the individual fiber strength. Molecular mechanisms responsible for regulating individual fiber strength remain unknown. Gossypium hirsutum near isogenic lines (NILs), MD52ne and MD90ne showing variations in BFS provide an opportunity for dissecting the regulatory mechanisms involved in individual fiber strength. Results Comprehensive fiber property analyses of the NILs revealed that the superior bundle strength of MD52ne fibers resulted from high individual fiber strength with minor contributions from greater fiber length. Comparative transcriptome analyses of the NILs showed that the superior bundle strength of MD52ne fibers was potentially related to two signaling pathways: one is ethylene and the interconnected phytohormonal pathways that are involved in cotton fiber elongation, and the other is receptor-like kinases (RLKs) signaling pathways that are involved in maintaining cell wall integrity. Multiple RLKs were differentially expressed in MD52ne fibers and localized in genomic regions encompassing the strength quantitative trait loci (QTLs). Several candidate genes involved in crystalline cellulose assembly were also up-regulated in MD52ne fibers while the secondary cell wall was produced. Conclusion Comparative phenotypic and transcriptomic analyses revealed differential expressions of the genes involved in crystalline cellulose assembly, ethylene and RLK signaling pathways between the MD52ne and MD90ne developing fibers. Ethylene and its phytohormonal network might promote the elongation of MD52ne fibers and indirectly contribute to the bundle strength by potentially improving fiber-to-fiber interactions. RLKs that were suggested to mediate a coordination of cell elongation and SCW biosynthesis in other plants might be candidate genes for regulating cotton fiber cell wall assembly and strength. Electronic supplementary material The online version of this article (doi:10.1186/s12870-016-0727-2) contains supplementary material, which is available to authorized users.
    Full-text · Article · Dec 2016
    • "The number of genes located in the four QTL of RPR and IVDMD were different from each other based on gene screening using qteller3 (http://qteller.com/qteller3/index.php) (Additional file 1: Table S5–S8). Nineteen genes have previously been demonstrated to be associated with cell wall formation mainly involved with cellulose and lignin synthesis (Table 5) [34][35][36][37][38][39][40][41][42][43]. Candidate genes participating same bioprocess were predicated between the DH and haploid populations for RPR and IVDMD, which were consistent with the results proposed by previous studies [20, 21, 44]. "
    [Show abstract] [Hide abstract] ABSTRACT: Background Doubled haploid (DH) lines produced via in vivo haploid induction have become indispensable in maize research and practical breeding, so it is important to understand traits characteristics in DH and its corresponding haploids which derived from each DH lines. In this study, a DH population derived from Zheng58 × Chang7-2 and a haploid population, were developed, genotyped and evaluated to investigate genetic architecture of eight stalk traits, especially rind penetrometer resistance (RPR) and in vitro dry matter digestion (IVDMD), which affecting maize stalk lodging-resistance and feeding values, respectively. Results Phenotypic correlation coefficients ranged from 0.38 to 0.69 between the two populations for eight stalk traits. Heritability values of all stalk traits ranged from 0.49 to 0.81 in the DH population, and 0.58 to 0.89 in the haploid population. Quantitative trait loci (QTL) mapping study showed that a total of 47 QTL for all traits accounting for genetic variations ranging from 1.6 to 36.5 % were detected in two populations. One or more QTL sharing common region for each trait were detected between two different ploidy populations. Potential candidate genes predicated from the four QTL support intervals for RPR and IVDMD were indirectly or directly involved with cellulose and lignin biosynthesis, which participated in cell wall formation. The increased expression levels of lignin and cellulose synthesis key genes in the haploid situation illustrated that dosage compensation may account for genome dosage effect in our study. Conclusions The current investigation extended understanding about the genetic basis of stalk traits and correlations between DH and its haploid populations, which showed consistence and difference between them in phenotype, QTL characters, and gene expression. The higher heritabilities and partly higher QTL detection power were presented in haploid population than in DH population. All of which described above could lay a preliminary foundation for genetic architecture study with haploid population and may benefit selection in haploid-stage to reduce cost in DH breeding. Electronic supplementary material The online version of this article (doi:10.1186/s12870-016-0742-3) contains supplementary material, which is available to authorized users.
    Full-text · Article · Dec 2016
    • "FEI2 was proposed to control cellulose biosynthesis with this function being redundant with FEI1 in roots (Xu et al., 2008). Multiple reports have also implicated FEI2 as a key component of a signaling pathway that can monitor cell wall conditions, and initiate a cytosolic response, specifically altering cellulose biosynthesis (Xu et al., 2008; Steinwand et al., 2014; Basu et al., 2016). Yet the evidence supporting a role for FEI2 in cellulose biosynthesis is not convincing. "
    [Show abstract] [Hide abstract] ABSTRACT: The plant cell wall is held together by the interactions between four major components: cellulose, pectin, hemicellulose, and proteins. Mucilage is a powerful model system to study the interactions between these components as it is formed of polysaccharides that are deposited in the apoplast of seed coat epidermal cells during seed development. When seeds are hydrated, these polysaccharides expand rapidly out of the apoplastic pocket, and form an adherent halo of mucilage around the seed. In Arabidopsis, mutations in multiple genes have similar loss of mucilage adherence phenotypes including CELLULOSE SYNTHASE 5 (CESA5)/MUCILAGE-MODIFIED 3 (MUM3), MUM5/MUCI21, SALT-OVERLY SENSITIVE 5 (SOS5), and FEI2. Here, we examine the interactions between these factors to better understand how they participate to control mucilage adherence. Double mutant phenotypes indicated that MUM5 and CESA5 function in a common mechanism that adheres pectin to the seed through the biosynthesis of cellulose and xylan, whereas SOS5 and FEI2, encoding a fasciclin-like arabinogalactan protein or a receptor-like kinase, respectively, function through an independent pathway. Cytological analyses of mucilage indicates that heteromannans are associated with cellulose, and not in the pathway involving SOS5 or FEI2. A SOS5 fluorescent protein fusion (SOS5-mCITRINE) was localized throughout the mucilage pocket, consistent with a structural role in pectin adhesion. The relationship between SOS5 and FEI2 mediated mucilage adherence was examined in more detail and while sos5 and fei2 mutants show similar phenotypes, key differences in the macromolecular characteristics and amounts of mucilage polymers were observed. FEI2 thus appears to have additional, as well as overlapping functions, with SOS5. Given that FEI2 is required for SOS5 function, we propose that FEI2 serves to localize SOS5 at the plasma membrane where it establishes interactions with mucilage polysaccharides, notably pectins, required for mucilage adherence prior to SOS5 being released into the apoplast.
    Full-text · Article · Aug 2016
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