Evolutionary Origins and Functions of the Carotenoid Biosynthetic Pathway in Marine Diatoms

被引:123
作者
Coesel, Sacha [1 ]
Obornik, Miroslav [2 ]
Varela, Joao [3 ]
Falciatore, Angela [1 ]
Bowler, Chris [1 ,4 ]
机构
[1] Stazione Zool Anton Dohrn, Cell Signalling Lab, Naples, Italy
[2] Univ S Bohemia, Acad Sci Czech Republic, Fac Sci, Biol Ctr, Inst Parasitol, Ceske Budejovice, Czech Republic
[3] Univ Algarve, Ctr Marine Sci, Faro, Portugal
[4] Ecole Normale Superieure, Dept Biol, CNRS UMR8186, Paris, France
关键词
D O I
10.1371/journal.pone.0002896
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Carotenoids are produced by all photosynthetic organisms, where they play essential roles in light harvesting and photoprotection. The carotenoid biosynthetic pathway of diatoms is largely unstudied, but is of particular interest because these organisms have a very different evolutionary history with respect to the Plantae and are thought to be derived from an ancient secondary endosymbiosis between heterotrophic and autotrophic eukaryotes. Furthermore, diatoms have an additional xanthophyll-based cycle for dissipating excess light energy with respect to green algae and higher plants. To explore the origins and functions of the carotenoid pathway in diatoms we searched for genes encoding pathway components in the recently completed genome sequences of two marine diatoms. Consistent with the supplemental xanthophyll cycle in diatoms, we found more copies of the genes encoding violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP) enzymes compared with other photosynthetic eukaryotes. However, the similarity of these enzymes with those of higher plants indicates that they had very probably diversified before the secondary endosymbiosis had occurred, implying that VDE and ZEP represent early eukaryotic innovations in the Plantae. Consequently, the diatom chromist lineage likely obtained all paralogues of ZEP and VDE genes during the process of secondary endosymbiosis by gene transfer from the nucleus of the algal endosymbiont to the host nucleus. Furthermore, the presence of a ZEP gene in Tetrahymena thermophila provides the first evidence for a secondary plastid gene encoded in a heterotrophic ciliate, providing support for the chromalveolate hypothesis. Protein domain structures and expression analyses in the pennate diatom Phaeodactylum tricornutum indicate diverse roles for the different ZEP and VDE isoforms and demonstrate that they are differentially regulated by light. These studies therefore reveal the ancient origins of several components of the carotenoid biosynthesis pathway in photosynthetic eukaryotes and provide information about how they have diversified and acquired new functions in the diatoms.
引用
收藏
页数:16
相关论文
共 73 条
[1]   ProtTest: selection of best-fit models of protein evolution [J].
Abascal, F ;
Zardoya, R ;
Posada, D .
BIOINFORMATICS, 2005, 21 (09) :2104-2105
[2]   An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms [J].
Allen, Andrew E. ;
Vardi, Assaf ;
Bowler, Chris .
CURRENT OPINION IN PLANT BIOLOGY, 2006, 9 (03) :264-273
[3]   The genome of the diatom Thalassiosira pseudonana:: Ecology, evolution, and metabolism [J].
Armbrust, EV ;
Berges, JA ;
Bowler, C ;
Green, BR ;
Martinez, D ;
Putnam, NH ;
Zhou, SG ;
Allen, AE ;
Apt, KE ;
Bechner, M ;
Brzezinski, MA ;
Chaal, BK ;
Chiovitti, A ;
Davis, AK ;
Demarest, MS ;
Detter, JC ;
Glavina, T ;
Goodstein, D ;
Hadi, MZ ;
Hellsten, U ;
Hildebrand, M ;
Jenkins, BD ;
Jurka, J ;
Kapitonov, VV ;
Kröger, N ;
Lau, WWY ;
Lane, TW ;
Larimer, FW ;
Lippmeier, JC ;
Lucas, S ;
Medina, M ;
Montsant, A ;
Obornik, M ;
Parker, MS ;
Palenik, B ;
Pazour, GJ ;
Richardson, PM ;
Rynearson, TA ;
Saito, MA ;
Schwartz, DC ;
Thamatrakoln, K ;
Valentin, K ;
Vardi, A ;
Wilkerson, FP ;
Rokhsar, DS .
SCIENCE, 2004, 306 (5693) :79-86
[4]   Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae [J].
Berges, JA ;
Charlebois, DO ;
Mauzerall, DC ;
Falkowski, PG .
PLANT PHYSIOLOGY, 1996, 110 (02) :689-696
[5]   Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii [J].
Bohne, F ;
Linden, H .
BIOCHIMICA ET BIOPHYSICA ACTA-GENE STRUCTURE AND EXPRESSION, 2002, 1579 (01) :26-34
[6]   Xanthophyll biosynthesis - Cloning, expression, functional reconstitution, and regulation of beta-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum) [J].
Bouvier, F ;
dHarlingue, A ;
Hugueney, P ;
Marin, E ;
MarionPoll, A ;
Camara, B .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1996, 271 (46) :28861-28867
[7]   Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli [J].
Bugos, RC ;
Yamamoto, HY .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1996, 93 (13) :6320-6325
[8]   Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants [J].
Bugos, RC ;
Hieber, AD ;
Yamamoto, HY .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1998, 273 (25) :15321-15324
[9]   EUKARYOTE KINGDOMS - 7 OR 9 [J].
CAVALIERSMITH, T .
BIOSYSTEMS, 1981, 14 (3-4) :461-481
[10]   Identification, expression, and evolutionary analyses of plant lipocalins [J].
Charron, JBF ;
Ouellet, F ;
Pelletier, M ;
Danyluk, J ;
Chauve, C ;
Sarhan, F .
PLANT PHYSIOLOGY, 2005, 139 (04) :2017-2028