Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors

被引:173
作者
Kubis, S
Patel, R
Combe, J
Bédard, J
Kovacheva, S
Lilley, K
Biehl, A
Leister, D
Ríos, G
Koncz, C
Jarvis, P [1 ]
机构
[1] Univ Leicester, Dept Biol, Leicester LE1 7RH, Leics, England
[2] Univ Cambridge, Cambridge Ctr Proteom, Cambridge CB2 1QW, England
[3] Max Planck Inst Zuchtungsforsch, D-50829 Cologne, Germany
关键词
D O I
10.1105/tpc.104.023309
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The initial stages of preprotein import into chloroplasts are mediated by the receptor GTPase Toc159. In Arabidopsis thaliana, Toc159 is encoded by a small gene family: atTOC159, atTOC132, atTOC120, and atTOC90. Phylogenetic analysis suggested that at least two distinct Toc159 subtypes, characterized by atToc159 and atToc132/atToc120, exist in plants. atTOC159 was strongly expressed in young, photosynthetic tissues, whereas atTOC132 and atTOC120 were expressed at a uniformly low level and so were relatively prominent in nonphotosynthetic tissues. Based on the albino phenotype of its knockout mutant, atToc159 was previously proposed to be a receptor with specificity for photosynthetic preproteins. To elucidate the roles of the other isoforms, we characterized Arabidopsis knockout mutants for each one. None of the single mutants had strong visible phenotypes, but toc132 toc120 double homozygotes appeared similar to toc159, indicating redundancy between atToc132 and atToc120. Transgenic complementation studies confirmed this redundancy but revealed little functional overlap between atToc132/atToc120 and atToc159 or atToc90. Unlike toc159, toc132 toc120 caused structural abnormalities in root plastids. Furthermore, when proteomics and transcriptomics were used to compare toc132 with ppi1 (a receptor mutant that is specifically defective in the expression, import, and accumulation of photosynthetic proteins), major differences were observed, suggesting that atToc132 (and atToc120) has specificity for nonphotosynthetic proteins. When both atToc159 and the major isoform of the other subtype, atToc132, were absent, an embryo-lethal phenotype resulted, demonstrating the essential role of Toc159 in the import mechanism.
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页码:2059 / 2077
页数:19
相关论文
共 54 条
[1]   Genome-wide Insertional mutagenesis of Arabidopsis thaliana [J].
Alonso, JM ;
Stepanova, AN ;
Leisse, TJ ;
Kim, CJ ;
Chen, HM ;
Shinn, P ;
Stevenson, DK ;
Zimmerman, J ;
Barajas, P ;
Cheuk, R ;
Gadrinab, C ;
Heller, C ;
Jeske, A ;
Koesema, E ;
Meyers, CC ;
Parker, H ;
Prednis, L ;
Ansari, Y ;
Choy, N ;
Deen, H ;
Geralt, M ;
Hazari, N ;
Hom, E ;
Karnes, M ;
Mulholland, C ;
Ndubaku, R ;
Schmidt, I ;
Guzman, P ;
Aguilar-Henonin, L ;
Schmid, M ;
Weigel, D ;
Carter, DE ;
Marchand, T ;
Risseeuw, E ;
Brogden, D ;
Zeko, A ;
Crosby, WL ;
Berry, CC ;
Ecker, JR .
SCIENCE, 2003, 301 (5633) :653-657
[2]   The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60α gene [J].
Apuya, NR ;
Yadegari, R ;
Fischer, RL ;
Harada, JJ ;
Zimmerman, JL ;
Goldberg, RB .
PLANT PHYSIOLOGY, 2001, 126 (02) :717-730
[3]   Unusual nucleotide-binding properties of the chloroplast protein import receptor, atToc33 [J].
Aronsson, H ;
Combe, J ;
Jarvis, P .
FEBS LETTERS, 2003, 544 (1-3) :79-85
[4]   A simple method for isolating import-competent Arabidopsis chloroplasts [J].
Aronsson, H ;
Jarvis, P .
FEBS LETTERS, 2002, 529 (2-3) :215-220
[5]   MITOCHONDRIAL PROTEINS ESSENTIAL FOR VIABILITY MEDIATE PROTEIN IMPORT INTO YEAST MITOCHONDRIA [J].
BAKER, KP ;
SCHATZ, G .
NATURE, 1991, 349 (6306) :205-208
[6]   Genetic diversity in Arabidopsis thaliana L. Heynh. investigated by cleaved amplified polymorphic sequence (CAPS) and inter-simple sequence repeat (ISSR) markers [J].
Barth, S ;
Melchinger, AE ;
Lübberstedt, T .
MOLECULAR ECOLOGY, 2002, 11 (03) :495-505
[7]   The major protein import receptor of plastids is essential for chloroplast biogenesis [J].
Bauer, J ;
Chen, KH ;
Hiltbunner, A ;
Wehrli, E ;
Eugster, M ;
Schnell, D ;
Kessler, F .
NATURE, 2000, 403 (6766) :203-207
[8]   Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane [J].
Bauer, J ;
Hiltbrunner, A ;
Weibel, P ;
Vidi, PA ;
Alvarez-Huerta, M ;
Smith, MD ;
Schnell, DJ ;
Kessler, F .
JOURNAL OF CELL BIOLOGY, 2002, 159 (05) :845-854
[9]   Preprotein recognition by the Toc complex [J].
Becker, T ;
Jelic, M ;
Vojta, A ;
Radunz, A ;
Soll, J ;
Schleiff, E .
EMBO JOURNAL, 2004, 23 (03) :520-530
[10]   A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide [J].
Bölter, B ;
May, T ;
Soll, J .
FEBS LETTERS, 1998, 441 (01) :59-62