Antagonistic roles of abscisic acid and cytokinin during response to nitrogen depletion in oleaginous microalga Nannochloropsis oceanica expand the evolutionary breadth of phytohormone function

被引:99
作者
Lu, Yandu [1 ]
Tarkowska, Danuse [2 ,3 ]
Tureckova, Veronika [2 ,3 ]
Luo, Tingwei [4 ]
Xin, Yi [1 ]
Li, Jing [1 ]
Wang, Qintao [1 ]
Jiao, Nianzhi [4 ]
Strnad, Miroslav [5 ]
Xu, Jian [1 ]
机构
[1] Chinese Acad Sci, Single Cell Ctr, Qingdao Inst BioEnergy & Bioprocess Technol, Chinese Acad Sci Key Lab Biofuels & Shandong Key, Qingdao 266101, Shandong, Peoples R China
[2] Palacky Univ, Lab Growth Regulators, Olomouc 78371, Czech Republic
[3] Inst Expt Bot AS CR, Olomouc 78371, Czech Republic
[4] Xiamen Univ, State Key Lab Marine Environm Sci, Xiamen 361000, Fujian, Peoples R China
[5] Palacky Univ, Fac Sci, Ctr Region Hana Biotechnol & Agr Res, Olomouc 78371, Czech Republic
关键词
Nannochloropsis oceanica; antagonistic synergy; abscisic acid; cytokinin; phytohormone evolution; stress response; cell-cycle progression; GENOME REVEALS; CHLAMYDOMONAS-REINHARDTII; ENDOGENOUS CYTOKININS; GREEN-ALGA; BIOSYNTHESIS; GROWTH; STRESS; SEQUENCE; DIVERSITY; MECHANISM;
D O I
10.1111/tpj.12615
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
The origin of phytohormones is poorly understood, and their physiological roles in microalgae remain elusive. Genome comparison of photosynthetic autotrophic eukaryotes has revealed that the biosynthetic pathways of abscisic acid (ABA) and cytokinins (CKs) emerged in unicellular algae. While ABA and CK degradation mechanisms emerged broadly in algal lineages, complete vascular plant-type conjugation pathways emerged prior to the rise of Streptophyta. In microalgae, a complete set of proteins from the canonical ABA and CK sensing and signaling pathways is not essential, but individual components are present, suggesting stepwise recruitment of phytohormone signaling components. In the oleaginous eustigmatophyte Nannochloropsis oceanica IMET1, UHPLC-MS/MS detected a wide array of plant hormones, despite a phytohormone profile that is very distinct from that of flowering plants. Time-series transcriptional analysis during nitrogen depletion revealed activation of the ABA biosynthetic pathway and antagonistic transcription of CK biosynthetic genes. Correspondingly, the ABA level increases while the dominant bioactive CK forms decrease. Moreover, exogenous CKs stimulate cell-cycle progression while exogenous ABA acts as both an algal growth repressor and a positive regulator in response to stresses. The presence of such functional flowering plant-like phytohormone signaling systems in Nannochloropsis sp. suggests a much earlier origin of phytohormone biosynthesis and degradation than previously believed, and supports the presence in microalgae of as yet unknown conjugation and sensing/signaling systems that may be exploited for microalgal feedstock development.
引用
收藏
页码:52 / 68
页数:17
相关论文
共 99 条
[1]   The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors [J].
Anantharaman, V ;
Aravind, L .
TRENDS IN BIOCHEMICAL SCIENCES, 2001, 26 (10) :579-582
[2]   The Puzzle of Plastid Evolution [J].
Archibald, John M. .
CURRENT BIOLOGY, 2009, 19 (02) :R81-R88
[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]   Plant carotenoid cleavage oxygenases and their apocarotenoid products [J].
Auldridge, Michele E. ;
McCarty, Donald R. ;
Klee, Harry J. .
CURRENT OPINION IN PLANT BIOLOGY, 2006, 9 (03) :315-321
[5]   Effects of brassinazole, an inhibitor of brassinosteroid biosynthesis, on light- and dark-grown Chlorella vulgaris [J].
Bajguz, A ;
Asami, T .
PLANTA, 2004, 218 (05) :869-877
[6]   Suppression of Chlorella vulgaris Growth by Cadmium, Lead, and Copper Stress and Its Restoration by Endogenous Brassinolide [J].
Bajguz, Andrzej .
ARCHIVES OF ENVIRONMENTAL CONTAMINATION AND TOXICOLOGY, 2011, 60 (03) :406-416
[7]  
Baldauf SL, 2008, J SYST EVOL, V46, P263, DOI 10.3724/SP.J.1002.2008.08008
[8]   The Selaginella Genome Identifies Genetic Changes Associated with the Evolution of Vascular Plants [J].
Banks, Jo Ann ;
Nishiyama, Tomoaki ;
Hasebe, Mitsuyasu ;
Bowman, John L. ;
Gribskov, Michael ;
dePamphilis, Claude ;
Albert, Victor A. ;
Aono, Naoki ;
Aoyama, Tsuyoshi ;
Ambrose, Barbara A. ;
Ashton, Neil W. ;
Axtell, Michael J. ;
Barker, Elizabeth ;
Barker, Michael S. ;
Bennetzen, Jeffrey L. ;
Bonawitz, Nicholas D. ;
Chapple, Clint ;
Cheng, Chaoyang ;
Correa, Luiz Gustavo Guedes ;
Dacre, Michael ;
DeBarry, Jeremy ;
Dreyer, Ingo ;
Elias, Marek ;
Engstrom, Eric M. ;
Estelle, Mark ;
Feng, Liang ;
Finet, Cedric ;
Floyd, Sandra K. ;
Frommer, Wolf B. ;
Fujita, Tomomichi ;
Gramzow, Lydia ;
Gutensohn, Michael ;
Harholt, Jesper ;
Hattori, Mitsuru ;
Heyl, Alexander ;
Hirai, Tadayoshi ;
Hiwatashi, Yuji ;
Ishikawa, Masaki ;
Iwata, Mineko ;
Karol, Kenneth G. ;
Koehler, Barbara ;
Kolukisaoglu, Uener ;
Kubo, Minoru ;
Kurata, Tetsuya ;
Lalonde, Sylvie ;
Li, Kejie ;
Li, Ying ;
Litt, Amy ;
Lyons, Eric ;
Manning, Gerard .
SCIENCE, 2011, 332 (6032) :960-963
[9]   Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana [J].
Bartrina, Isabel ;
Otto, Elisabeth ;
Strnad, Miroslav ;
Werner, Tomas ;
Schmuelling, Thomas .
PLANT CELL, 2011, 23 (01) :69-80
[10]   Cell-cycle regulation in green algae dividing by multiple fission [J].
Bisova, Katerina ;
Zachleder, Vilem .
JOURNAL OF EXPERIMENTAL BOTANY, 2014, 65 (10) :2585-2602