Complexes with Mixed Primary and Secondary Cellulose Synthases Are Functional in Arabidopsis Plants
2012
Carroll, Andrew | Mansoori, Nasim | Li, Shundai | Lei, Lei | Vernhettes, Samantha | Visser, Richard G. F. | Somerville, Chris | Gu, Ying | Trindade, Luisa M. | Dept Biol ; Stanford University | Energy Biosci Inst | Wageningen Univ, Lab Plant Breeding ; Wageningen University and Research [Wageningen] (WUR) | Grad Sch Expt Plant Sc ; Wageningen University and Research [Wageningen] (WUR) | Ctr LignoCellulose Struct & Format, Dept Biochem & Mol Bio ; Pennsylvania State University (Penn State) ; Penn State System-Penn State System | Institut Jean-Pierre Bourgin (IJPB) ; Institut National de la Recherche Agronomique (INRA)-AgroParisTech | Ctr LignoCellulose Struct & Format, Dept Biochem & Mol Biol ; Pennsylvania State University (Penn State) ; Penn State System-Penn State System | U.S. Department of Energy [DE-FG02-09ER16008]; Energy Biosciences Institute; Pennsylvania State University, Department of Biochemistry and Molecular Biology; Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center; U.S. Department of Energy, Office of Science [DE-SC0001090]
In higher plants, cellulose is synthesized by so-called rosette protein complexes with cellulose synthases (CESAs) as catalytic subunits of the complex. The CESAs are divided into two distinct families, three of which are thought to be specialized for the primary cell wall and three for the secondary cell wall. In this article, the potential of primary and secondary CESAs forming a functional rosette complex has been investigated. The membrane-based yeast two-hybrid and biomolecular fluorescence systems were used to assess the interactions between three primary (CESA1, CESA3, CESA6), and three secondary (CESA4, CESA7, CESA8) Arabidopsis (Arabidopsis thaliana) CESAs. The results showed that all primary CESAs can physically interact both in vitro and in planta with all secondary CESAs. Although CESAs are broadly capable of interacting in pairwise combinations, they are not all able to form functional complexes in planta. Analysis of transgenic lines showed that CESA7 can partially rescue defects in the primary cell wall biosynthesis in a weak cesa3 mutant. Green fluorescent protein-CESA protein fusions revealed that when CESA3 was replaced by CESA7 in the primary rosette, the velocity of the mixed complexes was slightly faster than the native primary complexes. CESA1 in turn can partly rescue defects in secondary cell wall biosynthesis in a cesa8ko mutant, resulting in an increase of cellulose content relative to cesa8ko. These results demonstrate that sufficient parallels exist between the primary and secondary complexes for cross-functionality and open the possibility that mixed complexes of primary and secondary CESAs may occur at particular times.
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