Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (Solanum lycopersicum)

被引:105
作者
Ariizumi, Tohru [1 ]
Kishimoto, Sanae [2 ]
Kakami, Ryo [1 ]
Maoka, Takashi [3 ]
Hirakawa, Hideki [4 ]
Suzuki, Yutaka [5 ]
Ozeki, Yuko [1 ]
Shirasawa, Kenta [4 ]
Bernillon, Stephane [6 ,7 ,8 ]
Okabe, Yoshihiro [1 ]
Moing, Annick [6 ,7 ,8 ]
Asamizu, Erika [4 ]
Rothan, Christophe [6 ,7 ]
Ohmiya, Akemi [2 ]
Ezura, Hiroshi [1 ]
机构
[1] Univ Tsukuba, Fac Life & Environm Sci, Tsukuba, Ibaraki 3058572, Japan
[2] NARO Inst Floricultural Sci, Tsukuba, Ibaraki 3058519, Japan
[3] Res Inst Prod Dev, Sakyo Ku, Kyoto 6060805, Japan
[4] Kazusa DNA Res Inst, Kisarazu 2920818, Japan
[5] Univ Tokyo, Grad Sch Frontier Sci, Dept Med Genome Sci, Kashiwa, Chiba 2778562, Japan
[6] INRA, F-33140 Villenave Dornon, France
[7] Univ Bordeaux, Unite Mixte Rech 1332, Biol Fruit & Pathol, F-33140 Villenave Dornon, France
[8] Ctr INRA Bordeaux, Plateforme Metabol Ctr Genom Fonct Bordeaux, F-33140 Villenave Dornon, France
关键词
Carotenoids; Solanum lycopersicum; xanthophyll; chromoplast; plastoglobule; gene cloning; esterification; ABSCISIC-ACID BIOSYNTHESIS; PAPRIKA CAPSICUM-ANNUUM; CHRYSANTHEMUM PETALS; ARABIDOPSIS-THALIANA; MICRO-TOM; FRUIT; DIOXYGENASE; CHROMOPLAST; ACCUMULATION; ESTERS;
D O I
10.1111/tpj.12570
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Xanthophylls, the pigments responsible for yellow to red coloration, are naturally occurring carotenoid compounds in many colored tissues of plants. These pigments are esterified within the chromoplast; however, little is known about the mechanisms underlying their accumulation in flower organs. In this study, we characterized two allelic tomato (Solanum lycopersicum L.) mutants, pale yellow petal (pyp) 1-1 and pyp1-2, that have reduced yellow color intensity in the petals and anthers due to loss-of-function mutations. Carotenoid analyses showed that the yellow flower organs of wild-type tomato contained high levels of xanthophylls that largely consisted of neoxanthin and violaxanthin esterified with myristic and/or palmitic acids. Functional disruption of PYP1 resulted in loss of xanthophyll esters, which was associated with a reduction in the total carotenoid content and disruption of normal chromoplast development. These findings suggest that xanthophyll esterification promotes the sequestration of carotenoids in the chromoplast and that accumulation of these esters is important for normal chromoplast development. Next-generation sequencing coupled with map-based positional cloning identified the mutant alleles responsible for the pyp1 phenotype. PYP1 most likely encodes a carotenoid modifying protein that plays a vital role in the production of xanthophyll esters in tomato anthers and petals. Our results provide insight into the molecular mechanism underlying the production of xanthophyll esters in higher plants, thereby shedding light on a longstanding mystery.
引用
收藏
页码:453 / 465
页数:13
相关论文
共 66 条
  • [1] Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana
    Ariizumi, T
    Hatakeyama, K
    Hinata, K
    Inatsugi, R
    Nishida, I
    Sato, S
    Kato, T
    Tabata, S
    Toriyama, K
    [J]. PLANT JOURNAL, 2004, 39 (02) : 170 - 181
  • [2] Genetic suppression analysis in novel vacuolar processing enzymes reveals their roles in controlling sugar accumulation in tomato fruits
    Ariizumi, Tohru
    Higuchi, Kenji
    Arakaki, Shoko
    Sano, Tsunenori
    Asamizu, Erika
    Ezura, Hiroshi
    [J]. JOURNAL OF EXPERIMENTAL BOTANY, 2011, 62 (08) : 2773 - 2786
  • [3] Plant carotenoid cleavage oxygenases and their apocarotenoid products
    Auldridge, Michele E.
    McCarty, Donald R.
    Klee, Harry J.
    [J]. CURRENT OPINION IN PLANT BIOLOGY, 2006, 9 (03) : 315 - 321
  • [4] Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes
    Austin, Jotham R., II
    Frost, Elizabeth
    Vidi, Pierre-Alexandre
    Kessler, Felix
    Staehelin, L. Andrew
    [J]. PLANT CELL, 2006, 18 (07) : 1693 - 1703
  • [5] Study of 'Redhaven' peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism
    Brandi, Federica
    Bar, Einat
    Mourgues, Fabienne
    Horvath, Gyoergyi
    Turcsi, Erika
    Giuliano, Giovanni
    Liverani, Alessandro
    Tartarini, Stefano
    Lewinsohn, Efraim
    Rosati, Carlo
    [J]. BMC PLANT BIOLOGY, 2011, 11
  • [6] Britton George., 2004, Carotenoids
  • [7] Biochemistry and molecular biology of chromoplast development
    Camara, B
    Hugueney, P
    Bouvier, F
    Kuntz, M
    Moneger, R
    [J]. INTERNATIONAL REVIEW OF CYTOLOGY, VOL 163, 1995, 163 : 175 - 247
  • [8] FREE AND ESTERIFIED CAROTENOIDS IN GREEN AND RED FRUITS OF CAPSICUM-ANNUUM
    CAMARA, B
    MONEGER, R
    [J]. PHYTOCHEMISTRY, 1978, 17 (01) : 91 - 93
  • [9] The Metabolic and Developmental Roles of Carotenoid Cleavage Dioxygenase4 from Potato
    Campbell, Raymond
    Ducreux, Laurence J. M.
    Morris, Wayne L.
    Morris, Jenny A.
    Suttle, Jeffrey C.
    Ramsay, Gavin
    Bryan, Glenn J.
    Hedley, Pete E.
    Taylor, Mark A.
    [J]. PLANT PHYSIOLOGY, 2010, 154 (02) : 656 - 664
  • [10] Formation and breakdown of ABA
    Cutler, AJ
    Krochko, JE
    [J]. TRENDS IN PLANT SCIENCE, 1999, 4 (12) : 472 - 478