TY - JOUR
T1 - TOPOISOMERASE 6B is involved in chromatin remodelling associated with control of carbon partitioning into secondary metabolites and cell walls, and epidermal morphogenesis in Arabidopsis
AU - Mittal, Amandeep
AU - Balasubramanian, Rajagopal
AU - Cao, Jin
AU - Singh, Prabhjeet
AU - Subramanian, Senthil
AU - Hicks, Glenn
AU - Nothnagel, Eugene A.
AU - Abidi, Noureddine
AU - Janda, Jaroslav
AU - Galbraith, David W.
AU - Rock, Christopher D.
N1 - Funding Information:
The authors thank Terry Thomas for providing the proDc3:GUS reporter lines 7-2 and 11-1, Ralph Quatrano for support, Lucy Smith for backcrossing hlq, the SEM facility at the Department of Pathology, University of Hong Kong for technical assistance with scanning electron microscopy, Thomas Altmann, Shibo Li, and Megan Sweeney for assistance with microarrays, Bruce Roe and Scott Dowd for preliminary sequencing and data analysis, respectively, Ruobai Sun for assistance with Illumina short read data sets, an anonymous reviewer for helpful suggestions on the manuscript, and the TTU High Performance Computing Center for support of the Hrothgar computer cluster. This work was supported by grant #2006-34186-16976-sub-J55-Q01097 from the USDA Southwest Consortium for Plant Genetics and Water Resources to CDR and DWG. The funders had no role in the study design, in the collection, analysis, or interpretation of data, or in the writing of the manuscript or decision to submit the manuscript for publication.
PY - 2014/8
Y1 - 2014/8
N2 - Plant growth is continuous and modular, a combination that allows morphogenesis by cell division and elongation and serves to facilitate adaptation to changing environments. The pleiotropic phenotypes of the harlequin (hlq) mutant, isolated on the basis of ectopic expression of the abscisic acid (ABA)-and auxin-inducible proDc3:GUS reporter gene, were previously characterized. Mutants are skotomorphogenic, have deformed and collapsed epidermal cells which accumulate callose and starch, cell walls abundant in pectins and cell wall proteins, and abnormal and reduced root hairs and leaf trichomes. hlq and two additional alleles that vary in their phenotypic severity of starch accumulation in the light and dark have been isolated, and it is shown that they are alleles of bin3/hyp6/rhl3/Topoisomerase6B. Mutants and inhibitors affecting the cell wall phenocopy several of the traits displayed in hlq. A microarray analysis was performed, and coordinated expression of physically adjacent pairs/sets of genes was observed in hlq, suggesting a direct effect on chromatin. Histones, WRKY and IAA/AUX transcription factors, aquaporins, and components of ubiquitin-E3-ligase-mediated proteolysis, and ABA or biotic stress response markers as well as proteins involved in cellular processes affecting carbon partitioning into secondary metabolites were also identified. A comparative analysis was performed of the hlq transcriptome with other previously published TopoVI mutant transcriptomes, namely bin3, bin5, and caa39 mutants, and limited concordance between data sets was found, suggesting indirect or genotype-specific effects. The results shed light on the molecular mechanisms underlying the det/cop/fus-like pleiotropic phenotypes of hlq and support a broader role for TopoVI regulation of chromatin remodelling to mediate development in response to environmental and hormonal signals.
AB - Plant growth is continuous and modular, a combination that allows morphogenesis by cell division and elongation and serves to facilitate adaptation to changing environments. The pleiotropic phenotypes of the harlequin (hlq) mutant, isolated on the basis of ectopic expression of the abscisic acid (ABA)-and auxin-inducible proDc3:GUS reporter gene, were previously characterized. Mutants are skotomorphogenic, have deformed and collapsed epidermal cells which accumulate callose and starch, cell walls abundant in pectins and cell wall proteins, and abnormal and reduced root hairs and leaf trichomes. hlq and two additional alleles that vary in their phenotypic severity of starch accumulation in the light and dark have been isolated, and it is shown that they are alleles of bin3/hyp6/rhl3/Topoisomerase6B. Mutants and inhibitors affecting the cell wall phenocopy several of the traits displayed in hlq. A microarray analysis was performed, and coordinated expression of physically adjacent pairs/sets of genes was observed in hlq, suggesting a direct effect on chromatin. Histones, WRKY and IAA/AUX transcription factors, aquaporins, and components of ubiquitin-E3-ligase-mediated proteolysis, and ABA or biotic stress response markers as well as proteins involved in cellular processes affecting carbon partitioning into secondary metabolites were also identified. A comparative analysis was performed of the hlq transcriptome with other previously published TopoVI mutant transcriptomes, namely bin3, bin5, and caa39 mutants, and limited concordance between data sets was found, suggesting indirect or genotype-specific effects. The results shed light on the molecular mechanisms underlying the det/cop/fus-like pleiotropic phenotypes of hlq and support a broader role for TopoVI regulation of chromatin remodelling to mediate development in response to environmental and hormonal signals.
KW - Anthocyanin
KW - cell wall
KW - endoreduplication
KW - hypocotyl
KW - light
KW - oxidative stress
KW - root hairless
KW - skotomorphogenesis
KW - starch
UR - http://www.scopus.com/inward/record.url?scp=84905197402&partnerID=8YFLogxK
U2 - 10.1093/jxb/eru198
DO - 10.1093/jxb/eru198
M3 - Article
C2 - 24821950
AN - SCOPUS:84905197402
SN - 0022-0957
VL - 65
SP - 4217
EP - 4239
JO - Journal of Experimental Botany
JF - Journal of Experimental Botany
IS - 15
ER -