Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening

被引:95
作者
Wang, Yuying [1 ]
Wang, Weihao [1 ,2 ]
Cai, Jianghua [1 ,2 ]
Zhang, Yanrui [1 ,2 ]
Qin, Guozheng [1 ]
Tian, Shiping [1 ,2 ]
机构
[1] Chinese Acad Sci, Inst Bot, Key Lab Plant Resources, Beijing 100093, Peoples R China
[2] Chinese Acad Sci, Grad Univ, Beijing 100049, Peoples R China
基金
中国国家自然科学基金;
关键词
26S PROTEASOME; GENE; EXPRESSION; ARABIDOPSIS; REGULATOR; PROTEINS; NETWORK; RIN; TRANSCRIPTOME; PATHWAY;
D O I
10.1186/s13059-014-0548-2
中图分类号
Q81 [生物工程学(生物技术)]; Q93 [微生物学];
学科分类号
071005 ; 0836 ; 090102 ; 100705 ;
摘要
Background: Fruits are unique to flowering plants and play a central role in seed maturation and dispersal. Molecular dissection of fruit ripening has received considerable interest because of the biological and dietary significance of fruit. To better understand the regulatory mechanisms underlying fruit ripening, we report here the first comprehensive analysis of the nuclear proteome in tomato fruits. Results: Nuclear proteins were isolated from tomatoes in different stages of ripening, and subjected to iTRAQ (isobaric tags for relative and absolute quantification) analysis. We show that the proteins whose abundances change during ripening stages are involved in various cellular processes. We additionally evaluate changes in the nuclear proteome in the ripening-deficient mutant, ripening-inhibitor (rin), carrying a mutation in the transcription factor RIN. A set of proteins were identified and particular attention was paid to SlUBC32 and PSMD2, the components of ubiquitin-proteasome pathway. Through chromatin immunoprecipitation and gel mobility shift assays, we provide evidence that RIN directly binds to the promoters of SlUBC32 and PSMD2. Moreover, loss of RIN function affects protein ubiquitination in nuclei. SlUBC32 encodes an E2 ubiquitin-conjugating enzyme and a genome-wide survey of the E2 gene family in tomatoes identified five more E2s as direct targets of RIN. Virus-induced gene silencing assays show that two E2s are involved in the regulation of fruit ripening. Conclusions: Our results uncover a novel function of protein ubiquitination, identifying specific E2s as regulators of fruit ripening. These findings contribute to the unraveling of the gene regulatory networks that control fruit ripening.
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页数:19
相关论文
共 73 条
[1]   Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development [J].
Alba, R ;
Payton, P ;
Fei, ZJ ;
McQuinn, R ;
Debbie, P ;
Martin, GB ;
Tanksley, SD ;
Giovannoni, JJ .
PLANT CELL, 2005, 17 (11) :2954-2965
[2]   Ubiquitylation in plants: a post-genomic look at a post-translational modification [J].
Bachmair, A ;
Novatchkova, M ;
Potuschak, T ;
Eisenhaber, F .
TRENDS IN PLANT SCIENCE, 2001, 6 (10) :463-470
[3]   Analysis of the Arabidopsis nuclear proteome and its response to cold stress [J].
Bae, MS ;
Cho, EJ ;
Choi, EY ;
Park, OK .
PLANT JOURNAL, 2003, 36 (05) :652-663
[4]   Regulation of chromatin by histone modifications [J].
Bannister, Andrew J. ;
Kouzarides, Tony .
CELL RESEARCH, 2011, 21 (03) :381-395
[5]   Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling [J].
Barry, Cornelius S. ;
Giovannoni, James J. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (20) :7923-7928
[6]  
Bateman A, 2004, NUCLEIC ACIDS RES, V32, pD138, DOI [10.1093/nar/gkp985, 10.1093/nar/gkh121, 10.1093/nar/gkr1065]
[7]   The Tomato FRUITFULL Homologs TDR4/FUL1 and MBP7/FUL2 Regulate Ethylene-Independent Aspects of Fruit Ripening [J].
Bemer, Marian ;
Karlova, Rumyana ;
Ballester, Ana Rosa ;
Tikunov, Yury M. ;
Bovy, Arnaud G. ;
Wolters-Arts, Mieke ;
Rossetto, Priscilla de Barros ;
Angenent, Gerco C. ;
de Maagd, Ruud A. .
PLANT CELL, 2012, 24 (11) :4437-4451
[8]   Chromatin techniques for plant cells [J].
Bowler, C ;
Benvenuto, G ;
Laflamme, P ;
Molino, D ;
Probst, AV ;
Tariq, M ;
Paszkowski, J .
PLANT JOURNAL, 2004, 39 (05) :776-789
[9]  
BRADFORD MM, 1976, ANAL BIOCHEM, V72, P248, DOI 10.1016/0003-2697(76)90527-3
[10]   PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order [J].
Caraux, G ;
Pinloche, S .
BIOINFORMATICS, 2005, 21 (07) :1280-1281