Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling
© Li et al.; licensee BioMed Central Ltd. 2014
Received: 20 December 2013
Accepted: 15 April 2014
Published: 23 April 2014
Salt stress usually causes crop growth inhibition and yield decrease. Epigenetic regulation is involved in plant responses to environmental stimuli. The epigenetic regulation of the cell wall related genes associated with the salt-induced cellular response is still little known. This study aimed to analyze cell morphological alterations in maize roots as a consequence of excess salinity in relation to the transcriptional and epigenetic regulation of the cell wall related protein genes.
In this study, maize seedling roots got shorter and displayed swelling after exposure to 200 mM NaCl for 48 h and 96 h. Cytological observation showed that the growth inhibition of maize roots was due to the reduction in meristematic zone cell division activity and elongation zone cell production. The enlargement of the stele tissue and cortex cells contributed to root swelling in the elongation zone. The cell wall is thought to be the major control point for cell enlargement. Cell wall related proteins include xyloglucan endotransglucosylase (XET), expansins (EXP), and the plasma membrane proton pump (MHA). RT-PCR results displayed an up-regulation of cell wall related ZmEXPA1, ZmEXPA3, ZmEXPA5, ZmEXPB1, ZmEXPB2 and ZmXET1 genes and the down-regulation of cell wall related ZmEXPB4 and ZmMHA genes as the duration of exposure was increased. Histone acetylation is regulated by HATs, which are often correlated with gene activation. The expression of histone acetyltransferase genes ZmHATB and ZmGCN5 was increased after 200 mM NaCl treatment, accompanied by an increase in the global acetylation levels of histones H3K9 and H4K5. ChIP experiment showed that the up-regulation of the ZmEXPB2 and ZmXET1 genes was associated with the elevated H3K9 acetylation levels on the promoter regions and coding regions of these two genes.
These data suggested that the up-regulation of some cell wall related genes mediated cell enlargement to possibly mitigate the salinity-induced ionic toxicity, and different genes had specific function in response to salt stress. Histone modification as a mediator may contribute to rapid regulation of cell wall related gene expression, which reduces the damage of excess salinity to plants.
KeywordsZea mays Cell enlargement Cell wall related genes Histone acetylation Root swelling Salt stress
Soil salinization owing to agricultural irrigation leads to crop growth rate reduction and yield decrease. The understanding of the mechanisms by which plants cope with high concentration of salt could enhance productivity in the high saline conditions. Excess NaCl inhibits plant growth both in shoots and roots . A significant growth reduction in the maize shoot and primary root is observed following NaCl treatment [2, 3]. One reason of the growth suppression is inadequate photosynthesis due to stomatal closure and consequently limited carbon dioxide uptake under salt stress  and thus most morphological and transcriptional studies on the effect of excess salinity have been focused on shoots and leaves because they are responsible for photosynthesis. But the effect of this stress on roots should be more obvious as the root is the organ that is directly exposed to the salinity soil . The molecular and cellular mechanism why the growth of young roots was repressed under salt stress is not precisely known.
The plant growth requires concerted water uptake and irreversible cell wall expansion to enlarge cells . The mechanical character of the cell wall controls the cell size and shape through the governance of cell expansion, which determines the morphology of tissues and organs . Several studies using transgenic materials have confirmed the role of expansins in promoting cell enlargement by affecting cell wall loosening [8, 9]. The plant cell wall is a dynamic network structure that consists of cellulose microfibrils and helicellulose embedded in a pectin matrix and contains proteins and numerous enzymes . This structure is important in plant growth and development and in response to various environmental stresses . The cell wall related proteins are believed to play a role in modulating cell wall extensibility that mediates cell enlargement and expansion. These proteins include xyloglucan endotransglucosylase (XET), endo-1,4-b-D-endoglucanase (EGase), expansins (EXP), and the plasma membrane proton pump (PM-H+-ATPase, MHA) . The low water potential is found to increase XET activity in the apical region of maize roots , although the possible role of XET in cell wall extension could not yet be confirmed in vitro . Expansins have been reported to induce immediate cell wall loosening in vitro and in vivo , and may be involved in acid-induced growth through disrupting the link between cellulose microfibrils and adjacent matrix . The expansin gene family that shares conserved motifs comprises four gene subfamilies: α-expansin (EXPA), β-expansin (EXPB), expansin-like A, and expansin-like B . The expansin gene expression level is highly related with the elongation growth of roots, internodes and leaves [8, 9, 18]. However, individual expansins are observed to be prior expressed in specific organs, which suggested that individual expansin genes had specific roles for plant development. PM-H+-ATPase can pump protons into the apoplast from the cytosol to acidify the apoplast where acidification activates expansin activity that in turn loosens the cell wall and expands cells . Xyloglucan is the most common hemicellulose in the primary cell wall in most plants. XET has been proposed as a potential cell wall extension protein because XET is able to cleave and rejoin xyloglucan chains . An up-regulation of the ZmXET1, ZmEXPA1, and ZmMHA mRNAs is found in maize shoots .
The gene expression is influenced by chromatin structure, which is dependent on epigenetic regulation, such as histone post-translational modifications and DNA methylation. The basic repeated unit of chromatin is the nucleosome in eukaryotes, which is formed by wrapping approximately 146 bp of DNA around a histone octamer that consists of two copies of each histone proteins, H2A, H2B, H3 and H4 . The N-terminus tail (N-tail) amino acid residue of the histones, exposed on the surface of the nucleosome, is subjected to post-translational modifications, including acetylation, methylation, phosphorylation and ubiquitination, catalyzed by histone modification enzymes [22, 23]. Histone acetyltransferases (HATs) are classified into two categories based on their subcellular distribution: the type A HATs and the type B HATs . Histone acetylation is regulated by HATs and often correlated with gene activation . Histone modification is involved in transcriptional regulation of many genes under salt stress [26, 27].
An understanding of the growth response of crop roots at cellular and molecular levels to salinity is of fundamental importance for a better comprehension of plant resistance to excess salinity and the breeding of salt stress-adapted crops. The cell wall is thought to be the major control point for cell enlargement, which is related with plant stress response. Currently, little is known about whether the histone modification is involved in regulating the expression of the cell wall related genes under salt stress conditions. This study aimed to analyze cell morphological alterations in maize roots as a consequence of excess salt in relation to the transcriptional and epigenetic regulation of the cell wall related protein genes. Salt stress induced maize growth inhibition along with root swelling and cell enlargement, which were accompanied by an up-regulation in some cell wall related genes. The global histone acetylation levels of H3K9 and H4K5 were increased in treated seedlings and the transcript levels of the ZmHATB and ZmGCN5 genes were increased, which might be an adaptive response of plants to salt stress. ChIP results displayed that up-regulation of the ZmEXPB2 and ZmXET1 genes was associated with an increase in histone H3K9 acetylation levels on the promoter regions and coding regions of these two genes in response to salt stress. Our data indicated that salt stress-induced elevation of H3K9Ac was accompanied by the change of cell well related gene expression, resulting in an adaptive cellular and growth response.
High salinity causes the elongation zone swelling and the meristematic zone shortening
High salinity activates the expression of HATs and increases global histone acetylation levels in the genome
High salinity selectively affects the expression of the cell-wall related genes
The local H3K9Ac levels of ZmEXPB2 and ZmXET1were increased under high-salinity stress
High salinity inhibited root growth and resulted in cell enlargement and root swelling
A high concentration of NaCl reduced root growth in many crop plants . In this study, 200 mM NaCl treatment caused maize growth inhibition, and the primary root length was significantly reduced. This was consistent with previous observations in maize and cotton seedling roots [2, 39]. The swelling elongation zone became wider and longer and the meristematic zone was reduced in length with the increasing of the treatment time with 200 mM NaCl (Figure 1B). Root swelling was also observed in maize roots exposed to salt stress  and aluminium stress [41, 42]. The formation of tuberized roots also has been reported in A.thaliana to be a consequence of drought stress  and salt stress [44, 45]. It has been reported the length of the meristematic zone of the primary root tips was reduced by 56% after 1 week of 1% NaCl treatment in A.thaliana. Our cytological analysis showed that the cortical cell radical enlargement after 200 mM NaCl treatment resulted in an increase in the root diameter. Similarly, a significant decline in the ratio of the cross-sectional area of the stele to area of the root was observed with increasing NaCl concentration in cotton roots . It has been reported that a radical swelling of all cell layers in root tips of Arabidopsis thaliana after 2 weeks of 1% NaCl stress . The length and volume of the cortical cells were increased, but the cell density in the cortex was significantly decreased, indicating that the cell production was decreased during salt stress. It has been reported that in cotton roots salinity diminished the rate of cell production . Burssens et al.  reported that the inhibition of A.thaliana root growth with salt stress is at least partially due to a decrease of cell production. The stele tissue cells transport water and soluble mineral nutrients from the roots to shoots. The transverse and radical enlargement of stele tissue cells was first emerged on the longitudinal section and the number of stele tissue cell layers was increased both in the transverse section and longitudinal section of the roots. These may help cells uptake more water and create more barrier to reduce Na+ concentration, which may be an adaptive mechanism to defense ionic toxicity. A decrease in the meristematic zone length of the primary root and the elongation zone cell numbers may be the reasons why the root growth was inhibited.
High salinity induced cell enlargement and root swelling in the elongation zone are accompanied by up-regulation of some cell wall related genes
The expression levels of expansin genes were increased in response to submergence in deepwater rice internode . The GmEXP1 expression level was very high in soybean roots where rapid root elongation took place and ectopic expression of GmEXP1 accelerated the growth of transgenic tobacco roots, which showed insensitivity to stress . Excised stem segments treated with auxin rapidly increased cell elongation, and the mRNAs of EXPA1, EXPA3, EXPA4 and EXPA5 were increased within 1 h . ExpB2 plays a role in the elongation of maize roots, and may be also involved in plant responses to environmental stimuli . It has been reported that the expression of EXP1, EXP5, EXP6 and EXP8 genes was up-regulated in maize primary roots after grown at low ψw, which likely contributed to enhanced cell wall extensibility and thus helped root cells maintain elongation at reduced turgor pressure . The expression of XET and expansins was about 100-fold higher in cotton fiber cells, corresponding to their proposed role in cell enlargement . The transcription levels of expansins and XET were increased after salt stress [50, 51]. The XET activity was enhanced in the apical region of maize roots from plants grown under low water potentials, and was suggested to be necessary for maintaining elongation . Our RT-PCR experiment showed that the transcript levels of ZmEXPA1, ZmEXPA3, ZmEXPA5, ZmEXPB1, ZmEXPB2 and ZmXET1 were increased from 2 to 96 h after exposure to high-salinity treatment. We presumed that the up-regulation of these five expansin genes and ZmXET1 was an adaptive mechanism to regulate the transverse and radical enlargement of the elongation zone cells, which may mitigate the decrease in root growth and the damage under high-salinity stress. It has been reported that the average cell length of mesocotyls was increased by up to 58% in the transgenic lines that overexpressed OsEXP4 . The ZmEXPB4 gene was down-regulated after treatment with 200 mM NaCl. Hormone treatment induced expression of Exp1 but repressed that of ExpB2 in maize roots . Therefore the differential expression patterns of expansins suggest that each expansin member may play a specific role in root growth and development, and in response to external stimuli. The acid growth theory thought that an auxin-induced acidic environment was needed for elongation growth . PM-H+-ATPase can pump protons into the apoplast from the cytosol to create a acidic environment and thus the down-regulation of ZmMHA may reduce root elongation growth.
Histone acetylation may be involved in high salinity-induced gene expression regulation
Recent studies have revealed that gene expression is regulated by dynamic histone modification, which could be an important mechanism for plants to adapt to abiotic stress [31, 54]. In tobacco BY2 and Arabidopsis T87 cells, high-salinity and cold stress triggered rapid up-regulation of histone H3 Ser-10 phosphorylation and histone H4 acetylation that was correlated with activation of stress-responsive genes . The mutations of GCN5 and ADA2 that encode the components of histone acetyltransferase complexes affected the expression of the cold stress-responsive genes in Arabidopsis . The enrichment of H3K9 acetylation and H3K4 trimethylation was related with the up-regulation of RD29A, RD29B, RD20, and RAP2.4 genes in response to drought treatment . Similarly, salt stress enriched H3K9K14 acetylation and H3K4 trimethylation on the promoter and coding regions of DREB2A, RD29A, and RD29B . Our results showed that the total acetylation levels of H3K9 and H4K5 in the genome were increased after treatment with 200 mM NaCl and this increase could be associated with the enhanced expression of ZmHATB and ZmGCN5. Therefore overall histone acetylation level change is likely to be an adaptive response to salt stress at the epigenetic levels. It has been reported that the overall acetylation level alteration may be related with basal transcription and help rapid restoration of the acetylation level when the recruited HAT is removed . Our results diaplayed salt stress caused the up-regulation of ZmEXPB2 and ZmXET1 genes, which was accompanied with the elevated H3K9 acetylation levels on promoter regions and coding regions of these two genes. These data support the conclusion that epigenetic regulation plays a vital role in rapid regulation of gene expression in plant adaptive response to environmental stimuli [57, 58].
This study showed that the stele tissue and cortex cells were enlarged after treatment with 200 mM NaCl, which was associated with an up-regulation of cell wall related genes ZmEXPA1, ZmEXPA3, ZmEXPA5, ZmEXPB1, ZmEXPB2 and ZmXET1. The expression of histone acetyltransferase genes ZmHATB and ZmGCN5 was increased accompanied by an increase in the global acetylation levels of histones H3K9 and H4K5, suggesting that epigenetic regulation was involved in salt stress response. ChIP experiment further indicated that the up-regulation of ZmEXPB2 and ZmXET1 genes was associated with the elevated H3K9 acetylation levels on promoter regions and coding regions of these two genes. These data imply that an epigenetic control of the expression of the cell wall related genes in response to salt stress results in cell enlargement and root swelling which is an adaptive response.
Plant materials and treatments
Maize seeds (Zea mays L. hybrid line Huayu 5) were germinated in the dark at 25°C on cotton gauzes soaked in water on the glass dish, and then the seedlings of uniform size were transferred to hydroponic cultures in buckets containing 1/2 Hoagland’s nutrient solution in a controlled environment chamber under relative humidity of 70%, photoperiod of 14 h irradiance of 120 μmol m-2 s-1 with temperatures of 25°C and in the dark 10 h of 20°C respectively. The solutions were fully renewed every 2 days. After 6 days, when the seedlings with two leaves, 200 mM NaCl was added to nutrient solution to initiate the saline treatment. Six-day-old maize seedlings grown in 1/2 Hoagland’s nutrient solution without NaCl were considered as a control group.
Six-day-old maize seedlings were transferred to nutrient solution supplemented with 0, 25, 50, 100, 150, 200 and 250 mM NaCl respectively for 7 days, then the image was obtained by Nikon J1 (Nikon Corporation, Japan). Six-day-old maize seedlings (n = 20) were transferred to nutrient solution supplemented with or without 200 mM NaCl treatment for 0, 2, 4, 8, 16, 24, 48 and 96 h, then maize seedlings were photographed by Nikon J1 (Nikon Corporation, Japan) and the primary root length and plant height were measured by Image J.
Root swelling and Feulgen staining
Feulgen staining of the primary roots was performed on 20 maize seedlings after 24, 48, 72 and 96 h treatment with nutrient solutions containing 0 (control) or 200 mM NaCl. Primary roots were fixed over night in a solution of ethanol and glacial acetic acid in a 3:1 ratio. Subsequently, roots were washed several times with 70% ethanol, followed by a gradual rehydration in increasing ethanol concentrations, 5 min per step with three changes of water at the end . Hydrolysis was performed in 1 N HCl for 15 min at 60°C, and stopped by replacing HCl with water. Root staining was achieved for 1 h in the dark at room temperature with Schiff’s Solution (Sigma, Taufkirchen, Germany) . After 1 h the roots were washed three times by deionized water and examined by Stereo Microscope (China) with 10X objective and 0.8X ocular. Images were captured by IScapture software (ISC, China) with a CCD monochrome camera (TCC-5.0, China).
For light microscopy studies, after a short rinse (10 s) with distilled water, the tips (0–10 mm) from primary roots were excised from control and 200 mM NaCl treated seedlings after 48 h and 96 h of exposure to salt treatment. The samples were immediately fixed with 3% glutaraldehyde and post fixed with 1% osmium tetroxide, dehydrated in ethanol series followed by embedded in Spurr’s resin. The transverse sections at approximately 5 mm from the apex and the longitudinal sections between 0 and 3 mm from apex were cut by ultramicrotome. Semi-thin transverse and longitudinal sections were stained with methylene blue (MB). Methylene blue stained specimens were examined with an Olympus BX-60 fluorescence microscope (Olympus, Tokyo, Japan) with bright-field illumination at 4X and 10X. Images were captured with a CCD monochrome camera Sensys 1401E and processed with ADOBE PHOTOSHOP 9.0 software (Adobe Systems, San Jose, CA).
The nuclei of maize roots were prepared in the slides according to the reported method . Immunostaining of the nuclei on the slides was carried out as described by Zhang et al. . The primary antibodies were H3K9Ac (catalog number: 07–352, Millipore, Billerica, MA, USA) and H4K5Ac (catalog number: 06–759, Millipore, Billerica, MA, USA) and the secondary antibody was fluorescein conjugated goat anti-rabbit IgG (catalog number: 12–507, Millipore, Billerica, MA USA). In control experiments, slides were incubated with the secondary antibody only. All slides were counterstained with 4,6-diamidino-2-phenylindole (DAPI, Sigma, USA), mounted with Vectashield (Vector labs, USA). Images were captured with a CCD monochrome camera Sensys 1401E under an Olympus BX-60 fluorescence microscope with filter blocks for DAPI and fluorescein, then pseudo-colored and merged using the software MetaMorph 7.7.2 (Universal Imaging Corp., USA). Microscope settings and camera detector exposure times were kept constant for the control and treated groups and more than 300 nuclei were analyzed. Images were processed using ADOBE PHOTOSHOP 9.0 software (Adobe Systems, San Jose, CA). The mean gray value of the immunostaining signals for H3K9Ac and H4K5Ac in the control and NaCl-treated samples was measured with Image J and MetaMorph. For both the control and treated groups, three independent immunostaining experiments were performed with each antibody. Mean gray value of the signal intensity and standard error of the mean value were calculated with SPSS10.0 for Windows package (SPSS Inc., 1999).
Western blot assay
Proteins were extracted from maize seedling roots by grinding in the liquid nitrogen and resuspended in the extraction buffer [100 mM Tris–HCl pH 7.4, 50 mM NaCl, 5 mM ethylenediaminetetraacetic acid (EDTA) and 1 mM phenylmethanesulfonyl fluoride (PMSF)]. Western blot detection was carried out as described by Yang et al. . Proteins were fractionated by SDS-PAGE and transferred to Immobilon-P membranes which were respectively incubated with the primary antibodies H3 (catalog number: 06–755, Upstate, Lake Placid, NY, USA), H3K9Ac and H4K5Ac overnight at 4°C. Detection was performed using alkaline phosphatase (AP) conjugated anti-rabbit IgG antibody and chemiluminescence visualization. Histone H3 was applied as an equal loading control. Densitometric measurements were taken after immunodetection using Image J. Abundance index was calculated as follows: H3K9Ac or H4K5Ac band intensity/H3 band intensity. Western blots were repeated three times for each sample from three independent experiments. Mean abundance index and standard error of the mean were calculated with SPSS10.0 for Windows package (SPSS Inc., 1999).
Quantitative real-time PCR
RT-PCR primer pairs for maize (Zea mays L.)
Chromatin immunoprecipitation (ChIP)
ChIP-PCR primer pairs for maize (Zea mays L.)
Product length (bp)
The accession numbers for the genes described in this paper are HATB [GRMZM5G851405_T02], GCN5 [GRMZM2G046021_T01], XET1 [GRMZM2G026980_T02], MHA [GRMZM2G148374_T01, GRMZM2G019404_T02, GRMZM2G450055_T01, GRMZM2G006894_T01], EXPA1 [GRMZM2G339122_T01], EXPA3 [GRMZM2G074585_T02], EXPA5 [GRMZM2G019398_T01], EXPB1 [GRMZM2G146551_T02], EXPB2 [GRMZM2G021621_T02], EXPB4 [GRMZM2G154178_T01], and Actin [GRMZM2G126010_T01].
We thank the anonymous reviewers for critical reading and constructive suggestions on improving the quality of this manuscript. This work was supported by the NSFC (No. 31171186) and Hubei Province Natural Science Fund.
- Katsuhara M, Kawasaki T: Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol. 1996, 37 (2): 169-173. 10.1093/oxfordjournals.pcp.a028928.View ArticleGoogle Scholar
- Zidan I, Azaizeh H, Neumann PM: Does salinity reduce growth in maize root epidermal cells by inhibiting their capacity for cell wall acidification?. Plant Physiol. 1990, 93 (1): 7-11. 10.1104/pp.93.1.7.PubMed CentralView ArticlePubMedGoogle Scholar
- Geilfus C-M, Zörb C, Mühling KH: Salt stress differentially affects growth-mediating β-expansins in resistant and sensitive maize (Zea mays L.). Plant Physiol Biochem. 2010, 48 (12): 993-998. 10.1016/j.plaphy.2010.09.011.View ArticlePubMedGoogle Scholar
- Ben Taarit M, Msaada K, Hosni K, Hammami M, Kchouk ME, Marzouk B: Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Ind Crops Prod. 2009, 30 (3): 333-337. 10.1016/j.indcrop.2009.06.001.View ArticleGoogle Scholar
- Hajibagheri M, Yeo A, Flowers T: Salt tolerance in Suaeda maritima (L.) Dum. Fine structure and ion concentrations in the apical region of roots. New Phytol. 1985, 99 (3): 331-343. 10.1111/j.1469-8137.1985.tb03661.x.View ArticleGoogle Scholar
- Cosgrove DJ: Water uptake by growing cells: an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int J Plant Sci. 1993, 154 (1): 10-21. 10.1086/297087.View ArticlePubMedGoogle Scholar
- Cosgrove DJ: Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell. 1997, 9 (7): 1031-10.1105/tpc.9.7.1031.PubMed CentralView ArticlePubMedGoogle Scholar
- Choi D, Lee Y, Cho H-T, Kende H: Regulation of expansin gene expression affects growth and development in transgenic rice plants. The Plant Cell Online. 2003, 15 (6): 1386-1398.View ArticleGoogle Scholar
- Cho H-T, Cosgrove DJ: Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci. 2000, 97 (17): 9783-9788. 10.1073/pnas.160276997.PubMed CentralView ArticlePubMedGoogle Scholar
- Cosgrove DJ: Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol. 1997, 13 (1): 171-201. 10.1146/annurev.cellbio.13.1.171.View ArticlePubMedGoogle Scholar
- Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB: Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J. 2006, 4 (2): 145-167. 10.1111/j.1467-7652.2005.00169.x.View ArticlePubMedGoogle Scholar
- Geilfus C-M, Zörb C, Neuhaus C, Hansen T, Lüthen H, Mühling KH: Differential transcript expression of wall-loosening candidates in leaves of maize cultivars differing in salt resistance. J Plant Growth Regul. 2011, 30 (4): 387-395. 10.1007/s00344-011-9201-4.View ArticleGoogle Scholar
- Wu Y, Spollen WG, Sharp RE, Hetherington PR, Fry SC: Root growth maintenance at low water potentials (increased activity of xyloglucan endotransglycosylase and its possible regulation by abscisic acid). Plant Physiol. 1994, 106 (2): 607-615.PubMed CentralPubMedGoogle Scholar
- McQueen-Mason SJ, Fry SC, Durachko DM, Cosgrove DJ: The relationship between xyloglucan endotransglycosylase and in-vitro cell wall extension in cucumber hypocotyls. Planta. 1993, 190 (3): 327-331.View ArticlePubMedGoogle Scholar
- Cosgrove DJ: Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Biol. 1999, 50 (1): 391-417. 10.1146/annurev.arplant.50.1.391.View ArticleGoogle Scholar
- McQueen-Mason S, Cosgrove DJ: Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci U S A. 1994, 91 (14): 6574-6578. 10.1073/pnas.91.14.6574.PubMed CentralView ArticlePubMedGoogle Scholar
- Sampedro J, Cosgrove DJ: The expansin superfamily. Genome Biol. 2005, 6 (12): 242-10.1186/gb-2005-6-12-242.PubMed CentralView ArticlePubMedGoogle Scholar
- Lee D-K, Ahn JH, Song S-K, Do Choi Y, Lee JS: Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol. 2003, 131 (3): 985-997. 10.1104/pp.009902.PubMed CentralView ArticlePubMedGoogle Scholar
- Moriau L, Michelet B, Bogaerts P, Lambert L, Michel A, Oufattole M, Boutry M: Expression analysis of two gene subfamilies encoding the plasma membrane H + -ATPase in Nicotiana plumbaginifolia reveals the major transport functions of this enzyme. Plant J. 1999, 19 (1): 31-41. 10.1046/j.1365-313X.1999.00495.x.View ArticlePubMedGoogle Scholar
- Fry S, Smith R, Renwick K, Martin D, Hodge S, Matthews K: Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J. 1992, 282: 821-828.PubMed CentralView ArticlePubMedGoogle Scholar
- Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ: Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 1997, 389 (6648): 251-260. 10.1038/38444.View ArticlePubMedGoogle Scholar
- Strahl BD, Allis CD: The language of covalent histone modifications. Nature. 2000, 403 (6765): 41-45. 10.1038/47412.View ArticlePubMedGoogle Scholar
- Wu J, Grunstein M: 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci. 2000, 25 (12): 619-623. 10.1016/S0968-0004(00)01718-7.View ArticlePubMedGoogle Scholar
- Roth SY, Denu JM, Allis CD: Histone acetyltransferases. Annu Rev Biochem. 2001, 70 (1): 81-120. 10.1146/annurev.biochem.70.1.81.View ArticlePubMedGoogle Scholar
- Chen ZJ, Tian L: Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression. 2007, 1769 (5): 295-307.View ArticleGoogle Scholar
- Chen L-T, Luo M, Wang Y-Y, Wu K: Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot. 2010, 61 (12): 3345-3353. 10.1093/jxb/erq154.PubMed CentralView ArticlePubMedGoogle Scholar
- Sokol A, Kwiatkowska A, Jerzmanowski A, Prymakowska-Bosak M: Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta. 2007, 227 (1): 245-254. 10.1007/s00425-007-0612-1.View ArticlePubMedGoogle Scholar
- Apse MP, Aharon GS, Snedden WA, Blumwald E: Salt tolerance conferred by overexpression of a vacuolar Na+/H + antiport in Arabidopsis. Science. 1999, 285 (5431): 1256-1258. 10.1126/science.285.5431.1256.View ArticlePubMedGoogle Scholar
- Azaizeh H, Gunse B, Steudle E: Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiol. 1992, 99 (3): 886-894. 10.1104/pp.99.3.886.PubMed CentralView ArticlePubMedGoogle Scholar
- Kim J-M, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M: Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol. 2008, 49 (10): 1580-1588. 10.1093/pcp/pcn133.View ArticlePubMedGoogle Scholar
- Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, Yang F, Huang M, Jiang L, Li L: Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One. 2011, 6 (7): e22132-10.1371/journal.pone.0022132.PubMed CentralView ArticlePubMedGoogle Scholar
- Li Y, Jones L, McQueen-Mason S: Expansins and cell growth. Curr Opin Plant Biol. 2003, 6 (6): 603-610. 10.1016/j.pbi.2003.09.003.View ArticlePubMedGoogle Scholar
- Zörb C, Noll A, Karl S, Leib K, Yan F, Schubert S: Molecular characterization of Na+/H + antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. J Plant Physiol. 2005, 162 (1): 55-66. 10.1016/j.jplph.2004.03.010.View ArticlePubMedGoogle Scholar
- Li B, Li N, Duan X, Wei A, Yang A, Zhang J: Generation of marker-free transgenic maize with improved salt tolerance using the FLP/FRT recombination system. J Biotechnol. 2010, 145 (2): 206-213. 10.1016/j.jbiotec.2009.11.010.View ArticlePubMedGoogle Scholar
- Wu Y, Thorne ET, Sharp RE, Cosgrove DJ: Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiol. 2001, 126 (4): 1471-1479. 10.1104/pp.126.4.1471.PubMed CentralView ArticlePubMedGoogle Scholar
- Cosgrove DJ, Bedinger P, Durachko DM: Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci. 1997, 94 (12): 6559-6564. 10.1073/pnas.94.12.6559.PubMed CentralView ArticlePubMedGoogle Scholar
- Kouzarides T: Chromatin modifications and their function. Cell. 2007, 128 (4): 693-705. 10.1016/j.cell.2007.02.005.View ArticlePubMedGoogle Scholar
- Liu T, Van Staden J, Cress W: Salinity induced nuclear and DNA degradation in meristematic cells of soybean (Glycine max (L.)) roots. Plant Growth Regul. 2000, 30 (1): 49-54. 10.1023/A:1006311619937.View ArticleGoogle Scholar
- Kurth E, Cramer GR, Läuchli A, Epstein E: Effects of NaCl and CaCl2 on cell enlargement and cell production in cotton roots. Plant Physiol. 1986, 82 (4): 1102-1106. 10.1104/pp.82.4.1102.PubMed CentralView ArticlePubMedGoogle Scholar
- Liang M, Haroldsen V, Cai X, Wu Y: Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress*. Plant Cell Environ. 2006, 29 (5): 746-753. 10.1111/j.1365-3040.2005.01435.x.View ArticlePubMedGoogle Scholar
- Blancaflor EB, Jones DL, Gilroy S: Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol. 1998, 118 (1): 159-172. 10.1104/pp.118.1.159.PubMed CentralView ArticlePubMedGoogle Scholar
- Ciamporová M: Diverse responses of root cell structure to aluminium stress. Plant Soil. 2000, 226 (1): 113-116. 10.1023/A:1026468403157.View ArticleGoogle Scholar
- Couot Gastelier J, Vartanian N: Drought-induced short roots in Arabidopsis thaliana: structural characteristics. Bot Acta. 1995, 108: 407-413. 10.1111/j.1438-8677.1995.tb00514.x.View ArticleGoogle Scholar
- Burssens S, Himanen K, Van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N: Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta. 2000, 211 (5): 632-640. 10.1007/s004250000334.View ArticlePubMedGoogle Scholar
- Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN: Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science. 2008, 320 (5878): 942-945. 10.1126/science.1153795.View ArticlePubMedGoogle Scholar
- Cho H-T, Kende H: Expression of expansin genes is correlated with growth in deepwater rice. The Plant Cell Online. 1997, 9 (9): 1661-1671. 10.1105/tpc.9.9.1661.View ArticleGoogle Scholar
- Jung J, O’Donoghue EM, Dijkwel PP, Brummell DA: Expression of multiple expansin genes is associated with cell expansion in potato organs. Plant Sci. 2010, 179 (1): 77-85.View ArticleGoogle Scholar
- Kam M-J, Yun HS, Kaufman PB, Chang SC: Two expansins, EXP1 and EXPB2, are correlated with the growth and development of maize roots. J Plant Biol. 2005, 48 (3): 304-310. 10.1007/BF03030527.View ArticleGoogle Scholar
- Ji SJ, Lu YC, Feng JX, Wei G, Li J, Shi YH, Fu Q, Liu D, Luo JC, Zhu YX: Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Res. 2003, 31 (10): 2534-2543. 10.1093/nar/gkg358.PubMed CentralView ArticlePubMedGoogle Scholar
- Ma S, Gong Q, Bohnert HJ: Dissecting salt stress pathways. J Exp Bot. 2006, 57 (5): 1097-1107. 10.1093/jxb/erj098.View ArticlePubMedGoogle Scholar
- Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt M-M, Klein PE: Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol. 2005, 58 (5): 699-720. 10.1007/s11103-005-7876-2.View ArticlePubMedGoogle Scholar
- Wu Y, Jeong B-R, Fry SC, Boyer JS: Change in XET activities, cell wall extensibility and hypocotyl elongation of soybean seedlings at low water potential. Planta. 2005, 220 (4): 593-601. 10.1007/s00425-004-1369-4.View ArticlePubMedGoogle Scholar
- Hager A: Role of the plasma membrane H + -ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res. 2003, 116 (6): 483-505. 10.1007/s10265-003-0110-x.View ArticlePubMedGoogle Scholar
- Zhao L, Wang P, Yan S, Gao F, Li H, Hou H, Zhang Q, Tan J, Li L: Promoter‒associated histone acetylation is involved in the osmotic stress‒induced transcriptional regulation of the maize ZmDREB2A gene. Physiol Plant. 2013, DOI: 10.1111/ppl.12136Google Scholar
- Vlachonasios KE, Thomashow MF, Triezenberg SJ: Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. The Plant Cell Online. 2003, 15 (3): 626-638. 10.1105/tpc.007922.View ArticleGoogle Scholar
- Vogelauer M, Wu J, Suka N, Grunstein M: Global histone acetylation and deacetylation in yeast. Nature. 2000, 408 (6811): 495-498. 10.1038/35044127.View ArticlePubMedGoogle Scholar
- Chinnusamy V, Zhu J-K: Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol. 2009, 12 (2): 133-139. 10.1016/j.pbi.2008.12.006.PubMed CentralView ArticlePubMedGoogle Scholar
- Luo M, Liu X, Singh P, Cui Y, Zimmerli L, Wu K: Chromatin modifications and remodeling in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms. 2012, 1819 (2): 129-136. 10.1016/j.bbagrm.2011.06.008.View ArticleGoogle Scholar
- Hoecker N, Keller B, Piepho H-P, Hochholdinger F: Manifestation of heterosis during early maize (Zea mays L.) root development. Theor Appl Genet. 2006, 112 (3): 421-429. 10.1007/s00122-005-0139-4.View ArticlePubMedGoogle Scholar
- De Tomasi J: Improving the technic of the Feulgen stain. Biotech Histochem. 1936, 11 (4): 137-144. 10.3109/10520293609110513.View ArticleGoogle Scholar
- Li L, Yang J, Tong Q, Zhao L, Song Y: A novel approach to prepare extended DNA fibers in plants. Cytometry A. 2005, 63 (2): 114-117.View ArticlePubMedGoogle Scholar
- Zhang L, Qiu Z, Hu Y, Yang F, Yan S, Zhao L, Li B, He S, Huang M, Li J: ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter‒associated histone acetylation. Physiol Plant. 2011, 143 (3): 287-296. 10.1111/j.1399-3054.2011.01496.x.View ArticlePubMedGoogle Scholar
- Yang F, Zhang L, Li J, Huang J, Wen R, Ma L, Zhou D, Li L: Trichostatin A and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol. 2010, 10 (1): 178-10.1186/1471-2229-10-178.PubMed CentralView ArticlePubMedGoogle Scholar
- Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M: Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods. 2007, 3 (1): 11-10.1186/1746-4811-3-11.PubMed CentralView ArticlePubMedGoogle Scholar
- Luo M, Wang Y-Y, Liu X, Yang S, Lu Q, Cui Y, Wu K: HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot. 2012, 63 (8): 3297-3306. 10.1093/jxb/ers059.PubMed CentralView ArticlePubMedGoogle Scholar
- Gendrel A-V, Lippman Z, Martienssen R, Colot V: Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods. 2005, 2 (3): 213-218. 10.1038/nmeth0305-213.View ArticlePubMedGoogle Scholar
- Saffery R, Sumer H, Hassan S, Wong LH, Craig JM, Todokoro K, Anderson M, Stafford A, Choo K: Transcription within a functional human centromere. Mol Cell. 2003, 12 (2): 509-516. 10.1016/S1097-2765(03)00279-X.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.