Antagonistic Peptide Technology for Functional Dissection of<i>CLV3/ESR</i>Genes in Arabidopsis

Song, Xiu‐Fen; Guo, Peng; Ren, Shi‐Chao; Xu, Tingting; Liu, Chunming

doi:10.1104/pp.112.211029

Cited by 65 publications

(70 citation statements)

References 46 publications

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“…The amino acid at position 6 of CLE peptides is crucial for their activity (15), and indeed, replacement of the corresponding glycine by threonine yielded a CLE45 variant (CLE45 G6T ) that had identical effects as the wild-type version but required application of higher peptide concentrations (Fig. 1K).…”

Section: Resultsmentioning

confidence: 99%

Molecular genetic framework for protophloem formation

Rodríguez-Villalón

Gujas

Kang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

169

286

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The phloem performs essential systemic functions in tracheophytes, yet little is known about its molecular genetic specification. Here we show that application of the peptide ligand CLAVATA3/EMBRYO SURROUNDING REGION 45 (CLE45) specifically inhibits specification of protophloem in Arabidopsis roots by locking the sieve element precursor cell in its preceding developmental state. CLE45 treatment, as well as viable transgenic expression of a weak CLE45 G6T variant, interferes not only with commitment to sieve element fate but also with the formative sieve element precursor cell division that creates protophloem and metaphloem cell files. However, the absence of this division appears to be a secondary effect of discontinuous sieve element files and subsequent systemically reduced auxin signaling in the root meristem. In the absence of the formative sieve element precursor cell division, metaphloem identity is seemingly adopted by the normally procambial cell file instead, pointing to possibly independent positional cues for metaphloem formation. The protophloem formation and differentiation defects in brevis radix (brx) and octopus (ops) mutants are similar to those observed in transgenic seedlings with increased CLE45 activity and can be rescued by loss of function of a putative CLE45 receptor, BARELY ANY MERI-STEM 3 (BAM3). Conversely, a dominant gain-of-function ops allele or mild OPS dosage increase suppresses brx defects and confers CLE45 resistance. Thus, our data suggest that delicate quantitative interplay between the opposing activities of BAM3-mediated CLE45 signals and OPS-dependent signals determines cellular commitment to protophloem sieve element fate, with OPS acting as a positive, quantitative master regulator of phloem fate. stem cell | division plane switching

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Section: Resultsmentioning

confidence: 99%

Molecular genetic framework for protophloem formation

Rodríguez-Villalón

Gujas

Kang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

169

286

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“…The jhs1 mutant plants were crossed with wild-type transgenic plants carrying ProWUS:GUS, ProCLV3:GUS, or ProSTM:GUS (Angela et al, 2002;Meng et al, 2012;Song et al, 2013), respectively. F 3 plants homozygous for the reporter gene and jhs1 were selected.…”

Section: Expression Pattern Analysis Of Sam-specific Genesmentioning

confidence: 99%

A DNA2 Homolog Is Required for DNA Damage Repair, Cell Cycle Regulation, and Meristem Maintenance in Plants

2016

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Plant meristem cells divide and differentiate in a spatially and temporally regulated manner, ultimately giving rise to organs. In this study, we isolated the Arabidopsis jing he sheng 1 (jhs1) mutant, which exhibited retarded growth, an abnormal pattern of meristem cell division and differentiation, and morphological defects such as fasciation, an irregular arrangement of siliques, and short roots. We identified JHS1 as a homolog of human and yeast DNA Replication Helicase/Nuclease2, which is known to be involved in DNA replication and damage repair. JHS1 is strongly expressed in the meristem of Arabidopsis. The jhs1 mutant was sensitive to DNA damage stress and had an increased DNA damage response, including increased expression of genes involved in DNA damage repair and cell cycle regulation, and a higher frequency of homologous recombination. In the meristem of the mutant plants, cell cycle progression was delayed at the G2 or late S phase and genes essential for meristem maintenance were misregulated. These results suggest that JHS1 plays an important role in DNA replication and damage repair, meristem maintenance, and development in plants.

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“…In addition, previous studies revealed that T-DNA insertion mutants of CLE1, CLE7, CLE10, CLE16, CLE18, or CLE19 in Arabidopsis exhibited no visible abnormal phenotype (Fiers et al, 2004;Jun et al, 2010), but overexpression of the CLE genes CLE2, CLE3, CLE4, CLE5, CLE6, CLE7, CLE10, CLE11, and CLE13 resulted in pleiotropic phenotypes similar to those of CLV3 or CLE40 overexpression plants, and in vitro application or overexpression of one of the CLE genes CLE19, CLE21, CLE25, CLE42, and CLE44 caused similar dwarf and short-root phenotypes (Fiers et al, 2004(Fiers et al, , 2005Strabala et al, 2006), suggesting a high level of functional redundancy or overlap among CLE members. Fortunately, an antagonistic peptide technology (Song et al, 2013) was developed recently as an effective tool to investigate the endogenous functions of these functionally redundant secreted peptides. Using CLV3 as a test case, Song et al (2013) examined the antagonistic peptide technology by transformations of wild-type Arabidopsis with constructs carrying the full-length CLV3 with every residue in the peptide-coding region replaced one at a time by Ala to probe the effectiveness of each mutation.…”

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confidence: 99%

“…Fortunately, an antagonistic peptide technology (Song et al, 2013) was developed recently as an effective tool to investigate the endogenous functions of these functionally redundant secreted peptides. Using CLV3 as a test case, Song et al (2013) examined the antagonistic peptide technology by transformations of wild-type Arabidopsis with constructs carrying the full-length CLV3 with every residue in the peptide-coding region replaced one at a time by Ala to probe the effectiveness of each mutation. They found that the Gly-to-Ala substitution in the core CLE motif caused a dominant-negative (DN) clv3-2-like phenotype.…”

mentioning

confidence: 99%

“…They found that the Gly-to-Ala substitution in the core CLE motif caused a dominant-negative (DN) clv3-2-like phenotype. Further substitutions of the Gly residue individually with the other 18 possible proteinaceous amino acids determined that the Gly-to-Thr substitution resulted in the strongest antagonistic effect in the wild type (Song et al, 2012(Song et al, , 2013. With this strategy, the peptide signal CLE19 was revealed to be important for cotyledon establishment in embryos and endosperm development (Xu et al, 2015).…”

mentioning

confidence: 99%

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Cytological and Transcriptomic Analyses Reveal Important Roles of CLE19 in Pollen Exine Formation

Wang

Song

et al. 2017

Plant Physiol.

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The CLAVATA3/ESR-RELATED (CLE) peptide signals are required for cell-cell communication in several plant growth and developmental processes. However, little is known regarding the possible functions of the CLEs in the anther. Here, we show that a T-DNA insertional mutant, and dominant-negative (DN) and overexpression (OX) transgenic plants of the CLE19 gene, exhibited significantly reduced anther size and pollen grain number and abnormal pollen wall formation in Arabidopsis (Arabidopsis thaliana). Interestingly, the DN-CLE19 pollen grains showed a more extensively covered surface, but CLE19-OX pollen exine exhibited clearly missing connections in the network and lacked separation between areas that normally form the lacunae. With a combination of cell biological, genetic, and transcriptomic analyses on cle19, DN-CLE19, and CLE19-OX plants, we demonstrated that CLE19-OX plants produced highly vacuolated and swollen aborted microspores (ams)-like tapetal cells, lacked lipidic tapetosomes and elaioplasts, and had abnormal pollen primexine without obvious accumulation of sporopollenin precursors. Moreover, CLE19 is important for the normal expression of more than 1,000 genes, including the transcription factor gene AMS, 280 AMS-downstream genes, and other genes involved in pollen coat and pollen exine formation, lipid metabolism, pollen germination, and hormone metabolism. In addition, the DN-CLE19(+/+) ams(2/2) plants exhibited the ams anther phenotype and ams(+/2) partially suppressed the DN-CLE19 transgeneinduced pollen exine defects. These findings demonstrate that the proper amount of CLE19 signal is essential for the normal expression of AMS and its downstream gene networks in the regulation of anther development and pollen exine formation.Pollen grains are generated in the male reproductive organ anther of flowering plants and are essential for plant fertility. In the model plant Arabidopsis (Arabidopsis thaliana), pollen grains are ellipsoidal, and the pollen surface is covered by a reticulate exine. In contrast, rice (Oryza sativa) pollen grains are globular and have a smooth surface without the reticulate structure. A well-organized pollen wall structure is essential for the physical and chemical stability of the mature pollen by providing protection for pollen grains from environmental stresses, such as desiccation and microbial attacks (Scott et al., 2004). The pollen wall is composed mainly of three layers: the intine layer, the exine layer, and the pollen coat (Zinkl et al., 1999;Edlund et al., 2004;Blackmore et al., 2007). The intine is the innermost layer of the pollen wall immediately adjacent to the plasma membrane of the pollen vegetative cell and is composed mainly of pectin, cellulose, hemicellulose, hydrolytic enzymes, and hydrophobic proteins (Scott et al., 2004). Both the exine layer and the pollen coat layer are basically of a lipidic nature. The exine is largely formed from acyl lipid and phenylpropanoid precursors, which together form the mixed stable biopolymer known as sporopollenin (Gui...

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Antagonistic Peptide Technology for Functional Dissection ofCLV3/ESRGenes in Arabidopsis

Cited by 65 publications

References 46 publications

Molecular genetic framework for protophloem formation

Molecular genetic framework for protophloem formation

A DNA2 Homolog Is Required for DNA Damage Repair, Cell Cycle Regulation, and Meristem Maintenance in Plants

Cytological and Transcriptomic Analyses Reveal Important Roles of CLE19 in Pollen Exine Formation

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