A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens

Goss, Chessa A.; Brockmann, Derek J.; Bushoven, John T.; Roberts, Alison W.

doi:10.1007/s00425-011-1579-5

Cited by 41 publications

(70 citation statements)

References 56 publications

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“…However, it is notable that the DEK1 Cys protease has been identified as a potential candidate involved in the initial proteolysis and turnover of CELLULOSE SYNTHASE A (CesA) in cotton (Gossypium hirsutum) rosettes (Jacob-Wilk et al, 2006) responsible for cellulose biosynthesis in primary and secondary cell walls (Festucci-Buselli et al, 2007). Both calcium signaling and CesA have been implicated in moss bud development (Saunders and Hepler, 1982;Goss et al, 2012). Cytokinin treatment induces bud formation, which coincides with elevated intracellular Ca…”

Section: Discussionmentioning

confidence: 99%

The DEK1 calpain Linker functions in three-dimensional body patterning in Physcomitrella patens

Johansen¹,

Ako²,

Demko

et al. 2016

Plant Physiol.

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The DEFECTIVE KERNEL1 (DEK1) calpain is a conserved 240-kD key regulator of three-dimensional body patterning in land plants acting via mitotic cell plane positioning. The activity of the cytosolic C-terminal calpain protease is regulated by the membrane-anchored DEK1 MEM, which is connected to the calpain via the 600-amino acid residue Linker. Similar to the calpain and MEM domains, the Linker is highly conserved in the land plant lineage, the similarity dropping sharply compared with orthologous charophyte sequences. Using site-directed mutagenesis, we studied the effect on Physcomitrella patens development by deleting the Linker and two conserved Linker motifs. The results show that removal of the Linker has nearly the same effect as removal of the entire DEK1 gene. In contrast, deletion of the conserved Laminin_G3 (LG3) domain had a milder effect, perturbing leafy gametophore patterning and archegonia development. The LG3 domain from Marchantia polymorpha is fully functional in P. patens, whereas angiosperm sequences are not functional. Deletion of a C-terminal Linker subsegment containing a potential calpain autolytic site severely disturbs gametophore development. Finally, changing one of the three calpain activesite amino acid residues results in the same phenotype as deleting the entire DEK1 gene. Based on the conserved nature of animal and DEK1 calpains, we propose that the DEK1 MEM-Linker complex inactivates the calpain by forcing apart the two calpain subunits carrying the three amino acids of the active site.The three-dimensional (3D) architecture of land plant bodies is determined by the orientation of cell walls deposited between dividing nuclei in developing organs. The ability to determine cell wall orientation in various planes was a novel feature that evolved in the transition from filamentous charophyte algae to the first land plants ( Pires and Dolan, 2012). In contrast to land plants, tip expansion and fixed division planes of the cells drove a two-dimensional (2D) growth pattern of charophyte members represented by filamentous or discoid forms. The membrane-anchored DEFECTIVE KERNEL1 (DEK1) calpain is a candidate protein involved in position-dependent cell wall deposition in the plant lineage (Perroud et al., 2014). Evidence for a conserved function in land plants comes from the observation that DEK1 is essential for cell wall orientation in land plants ranging from angiosperms to mosses, an evolutionary time span of 450 million years (Olsen et al., 2015). Support for a central function of DEK1 also comes from a recent review in which analyses of meristematic shoot tip transcriptomes of widely divergent extant vascular plant lineage members suggest that different genes were recruited to regulate similar meristematic processes during evolution. Exceptions identified include PIN-FORMED, DEK1, and LONELY GUY1 (Frank et al., 2015) proteins that represent potential genetic homologs in meristem function (Harrison, 2015).The DEK1 calpain derives its name from the maize (Zea mays) mutant dek1, whic...

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Section: Discussionmentioning

confidence: 99%

The DEK1 calpain Linker functions in three-dimensional body patterning in Physcomitrella patens

Johansen¹,

Ako²,

Demko

et al. 2016

Plant Physiol.

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“…When PpCESA5 was disrupted, gametophore buds failed to develop into leafy gametophores, instead forming irregular cell clumps. The associated disruptions of cell expansion and cell division are consistent with an underlying defect in primary cell wall deposition (Goss et al, 2012). Recently it was shown that PpCESA3 expression is regulated by the NAC transcription factor PpVNS7, along with the thickening of stereid cell walls (Xu et al, 2014).…”

mentioning

confidence: 71%

“…The formation of morphologically normal gametophores in ppcesa3/8KOs (Fig. 1) indicates that PpCESA3 and PpCESA8 serve a different role in development than PpCESA5, which supports the normal cell division and cell expansion required for gametophore development (Goss et al, 2012). It is possible that PpCESA3 and PpCESA8 contribute to primary cell wall Figure 6.…”

Section: Ppcesa3 and Ppcesa8 Function Redundantly In Cellulose Deposimentioning

confidence: 88%

“…In Arabidopsis, the secondary CESAs are AtCESA4, AtCESA7, and AtCESA8 (Taylor et al, 2003) and the primary CESAs are AtCESA1, AtCESA3, and members of the 6-like group (Desprez et al, 2007;Persson et al, 2007). In P. patens, midrib secondary cell wall synthesis involves PpCESA3, PpCESA6, PpCESA7, and PpCESA8, whereas gametophore primary cell wall synthesis requires PpCESA5 (Goss et al, 2012). At least some primary CESAs can substitute for secondary CESAs and vice versa in both species.…”

Section: Cesa Evolution In Both P Patens and Arabidopsis Involves Sumentioning

confidence: 99%

“…The moss Physcomitrella patens has seven CESA genes (Roberts and Bushoven, 2007;Goss et al, 2012). Phylogenetic analysis has revealed that the P. patens CESAs do not cluster with the six CESA clades shared by seed plants (Roberts and Bushoven, 2007).…”

mentioning

confidence: 99%

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Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants

Norris

Huang

et al. 2017

Plant Physiol.

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Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms

et al. 2021

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Understanding protein structure and function relationships in cellulose synthase (CesA), including divergent isomers, is an important goal. Here, we report results from mutant complementation assays that tested the ability of sequence variants of AtCesA7, a secondary wall CesA of Arabidopsis thaliana, to rescue the collapsed vessels, short stems, and low cellulose content of the irx3-1 AtCesA7 null mutant. We tested a catalytic null mutation and seven missense or small domain changes in and near the AtCesA7 FTVTSK motif, which lies near the catalytic domain and may, analogously to bacterial CesA, exist within a substrate "gating loop." A low-to-high gradient of rescue occurred, and even inactive AtCesA7 had a small positive effect on stem cellulose content but not stem elongation. Overall, secondary wall cellulose content and stem length were moderately correlated, but the results were consistent with threshold amounts of cellulose supporting particular developmental processes.Vibrational sum frequency generation microscopy allowed tissue-specific analysis of cellulose content in stem xylem and interfascicular fibers, revealing subtle differences between selected genotypes that correlated with the extent of rescue of the collapsing xylem phenotype. Similar tests on PpCesA5 from the moss Physcomitrium (formerly Physcomitrella) patens helped us to synergize the AtCesA7 results with prior results on AtCesA1 and PpCesA5. The cumulative results show that the FTVTxK region is important for the function of an angiosperm secondary wall CesA as well as widely divergent primary wall CesAs, while differences in complementation results between isomers may reflect functional differences that can be explored in further work.

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A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens

Cited by 41 publications

References 56 publications

The DEK1 calpain Linker functions in three-dimensional body patterning in Physcomitrella patens

The DEK1 calpain Linker functions in three-dimensional body patterning in Physcomitrella patens

Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants

Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms

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