Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana

BackgroundFormation of plant root hairs originating from epidermal cells involves selection of a polar initiation site and production of an initial hair bulge which requires local cell wall loosening. In Arabidopsis the polar initiation site is located towards the basal end of epidermal cells. However little is currently understood about the mechanism for the selection of the hair initiation site or the mechanism by which localised hair outgrowth is achieved. The Arabidopsis procuste1 (prc1-1) cellulose synthase mutant was studied in order to investigate the role of the cell wall loosening during the early stages of hair formation.ResultsThe prc1-1 mutant exhibits uncontrolled, preferential bulging of trichoblast cells coupled with mislocalised hair positioning. Combining the prc1-1 mutant with root hair defective6-1 (rhd6-1), which on its own is almost completely devoid of root hairs results in a significant restoration of root hair formation. The pEXPANSIN7::GFP (pEXP7::GFP) marker which is specifically expressed in trichoblast cell files of wild-type roots, is absent in the rhd6-1 mutant. However, pEXP7::GFP expression in the rhd6-1/prc1-1 double mutant is restored in a subset of epidermal cells which have either formed a root hair or exhibit a bulged phenotype consistent with a function for EXP7 during the early stages of hair formation.ConclusionThese results show that RHD6 acts upstream of the normal cell wall loosening event which involves EXP7 expression and that in the absence of a functional RHD6 the loosening and accompanying EXP7 expression is blocked. In the prc1-1 mutant background, the requirement for RHD6 during hair initiation is reduced which may result from a weaker cell wall structure mimicking the cell wall loosening events during hair formation.

[1]  J. Verbelen,et al.  Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. , 2001, Plant physiology.

[2]  D. Cosgrove,et al.  Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006437. , 2002, The Plant Cell Online.

[3]  W Herth,et al.  Molecular analysis of cellulose biosynthesis in Arabidopsis. , 1998, Science.

[4]  Paul Linstead,et al.  An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants , 2007, Science.

[5]  R. Williamson,et al.  The cellulose-deficient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glucosidase II, an enzyme processing N-glycans during ER quality control. , 2002, The Plant journal : for cell and molecular biology.

[6]  Staffan Persson,et al.  Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[7]  Samantha Vernhettes,et al.  A plasma membrane‐bound putative endo‐1,4‐β‐D‐glucanase is required for normal wall assembly and cell elongation in Arabidopsis , 1998, The EMBO journal.

[8]  J. Schiefelbein,et al.  Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. , 1996, The Plant cell.

[9]  Klaus Palme,et al.  Vectorial Information for Arabidopsis Planar Polarity Is Mediated by Combined AUX1, EIN2, and GNOM Activity , 2006, Current Biology.

[10]  Ying Fu,et al.  The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root Hair Initiation and Tip Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010359. , 2002, The Plant Cell Online.

[11]  Sandra Pelletier,et al.  Resistance against Herbicide Isoxaben and Cellulose Deficiency Caused by Distinct Mutations in Same Cellulose Synthase Isoform CESA61 , 2002, Plant Physiology.

[12]  R. Ridge Recent developments in the cell and molecular biology of root hairs , 1995, Journal of Plant Research.

[13]  C. Hocart,et al.  A mutation in an Arabidopsis ribose 5-phosphate isomerase reduces cellulose synthesis and is rescued by exogenous uridine. , 2006, The Plant journal : for cell and molecular biology.

[14]  A. Nakano,et al.  Arabidopsis Sterol Endocytosis Involves Actin-Mediated Trafficking via ARA6-Positive Early Endosomes , 2003, Current Biology.

[15]  T. Baskin,et al.  The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules , 2002, Planta.

[16]  D. Delmer,et al.  Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Caboche,et al.  Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation, respectively in dark- and light-grown Arabidopsis seedlings. , 1996, Development.

[18]  L. Dolan,et al.  Galactose Biosynthesis in Arabidopsis Genetic Evidence for Substrate Channeling from UDP-D-Galactose into Cell Wall Polymers , 2002, Current Biology.

[19]  K. Ljung,et al.  Cell Polarity Signaling in Arabidopsis Involves a BFA-Sensitive Auxin Influx Pathway , 2002, Current Biology.

[20]  Brad M. Binder,et al.  A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. , 1999, Science.

[21]  J. Friml,et al.  Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth , 2001, The EMBO journal.

[22]  Guislaine Refregier,et al.  PROCUSTE1 Encodes a Cellulose Synthase Required for Normal Cell Elongation Specifically in Roots and Dark-Grown Hypocotyls of Arabidopsis , 2000, Plant Cell.

[23]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[24]  K. Feldmann,et al.  T-DNA Insertion Mutagenesis in Arabidopsis: Prospects and Perspectives , 1992 .

[25]  K. Roberts,et al.  Growth Regulators and the Control of Nucleotide Sugar Flux , 2004, The Plant Cell Online.

[26]  S. Gilroy,et al.  Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. , 1998, Development.

[27]  T. Baskin,et al.  Root morphology mutants in Arabidopsis thaliana , 1992 .

[28]  M. Grebe Ups and downs of tissue and planar polarity in plants , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[29]  M. Braun,et al.  Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. , 2000, Developmental biology.

[30]  J. Schiefelbein,et al.  The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process , 1994, Plant physiology.

[31]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[32]  T. Baskin,et al.  Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-beta-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. , 2001, Plant physiology.

[33]  T. Baskin,et al.  The impact of mannose and other carbon sources on the elongation and diameter of the primary root of Arabidopsis thaliana , 2001 .

[34]  I. Szarejko,et al.  Molecular Cloning and Characterization of β-Expansin Gene Related to Root Hair Formation in Barley1 , 2006, Plant Physiology.

[35]  D. Jones,et al.  Through form to function: root hair development and nutrient uptake. , 2000, Trends in plant science.

[36]  N. Eckardt Cellulose Synthesis Takes the CesA Train , 2003, The Plant Cell Online.

[37]  L. Dolan,et al.  Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. , 1995, The Plant journal : for cell and molecular biology.

[38]  Alan Marchant,et al.  AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues , 1999, The EMBO journal.