A Functional Genomics View of Gibberellin Metabolism in the Cnidarian Symbiont Breviolum minutum

. 2022 ; 13 () : 927200. [epub] 20220912

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36172550

Dinoflagellate inhabitants of the reef-building corals exchange nutrients and signals with host cells, which often benefit the growth of both partners. Phytohormones serve as central hubs for signal integration between symbiotic microbes and their hosts, allowing appropriate modulation of plant growth and defense in response to various stresses. However, the presence and function of phytohormones in photosynthetic dinoflagellates and their function in the holobionts remain elusive. We hypothesized that endosymbiotic dinoflagellates may produce and employ phytohormones for stress responses. Using the endosymbiont of reef corals Breviolum minutum as model, this study aims to exam whether the alga employ analogous signaling systems by an integrated multiomics approach. We show that key gibberellin (GA) biosynthetic genes are widely present in the genomes of the selected dinoflagellate algae. The non-13-hydroxylation pathway is the predominant route for GA biosynthesis and the multifunctional GA dioxygenase in B. minutum has distinct substrate preference from high plants. GA biosynthesis is modulated by the investigated bleaching-stimulating stresses at both transcriptional and metabolic levels and the exogenously applied GAs improve the thermal tolerance of the dinoflagellate. Our results demonstrate the innate ability of a selected Symbiodiniaceae to produce the important phytohormone and the active involvement of GAs in the coordination and the integration of the stress response.

Zobrazit více v PubMed

Aranda M., Li Y., Liew Y. J., Baumgarten S., Simakov O., Wilson M. C. (2016). Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. PubMed DOI PMC

Claeys H., De Bodt S., Inzé D. (2014). Gibberellins and DELLAs: central nodes in growth regulatory networks. PubMed DOI

Davy S. K., Allemand D., Weis V. M. (2012). Cell biology of cnidarian-dinoflagellate symbiosis. PubMed DOI PMC

Gan Q., Zhou W., Wang S., Li X., Xie Z., Wang J., et al. (2017). A customized contamination controlling approach for culturing oleaginous Nannochloropsis oceanica.

González-Garcinuño Á, Sánchez-Álvarez J. M., Galán M. A., Martin Del Valle E. M. (2016). Understanding and optimizing the addition of phytohormones in the culture of microalgae for lipid production. PubMed DOI

Han X., Song X., Li F., Lu Y. (2020). Improving lipid productivity by engineering a control-knob gene in the oleaginous microalga Nannochloropsis oceanica. PubMed DOI PMC

Helliwell C. A., Poole A., Peacock W. J., Dennis E. S. (1999). Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. PubMed DOI PMC

Hu Y., Zhou L., Huang M., He X., Yang Y., Liu X., et al. (2018). Gibberellins play an essential role in late embryogenesis of Arabidopsis. PubMed DOI

Israelsson M., Mellerowicz E., Chono M., Gullberg J., Moritz T. (2004). Cloning and overproduction of gibberellin 3-oxidase in hybrid aspen trees. effects on gibberellin homeostasis and development. PubMed DOI PMC

Jeong H. J., Yoo Y. D., Kang N. S., Lim A. S., Seong K. A., Lee S. Y., et al. (2012). Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. PubMed DOI PMC

Jiang J., Lu Y. (2019). Metabolite profiling of Breviolum minutum in response to acidification. PubMed DOI

Jiang J., Wang A., Deng X., Zhou W., Gan Q., Lu Y. (2021). How Symbiodiniaceae meets the challenges of life during coral bleaching.

Kapoore R. V., Wood E. E., Llewellyn C. A. (2021). Algae biostimulants: a critical look at microalgal biostimulants for sustainable agricultural practices. PubMed DOI

Kopp C., Domart-Coulon I., Escrig S., Humbel B. M., Hignette M., Meibom A. (2015). Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. PubMed DOI PMC

Lajeunesse T. C., Parkinson J. E., Gabrielson P. W., Jeong H. J., Reimer J. D., Voolstra C. R., et al. (2018). Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. PubMed DOI

Lange T., Hedden P., Graebe J. E. (1994). Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. PubMed DOI PMC

Lin S., Cheng S., Song B., Zhong X., Lin X., Li W., et al. (2015). The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. PubMed DOI

Liu H., Stephens T. G., González-Pech R. A., Beltran V. H., Lapeyre B., Bongaerts P. (2018). Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. PubMed PMC

Lu Y., Zhang X., Gu X., Lin H., Melis A. (2021b). Engineering microalgae: transition from empirical design to programmable cells. PubMed DOI

Lu Y., Gan Q., Iwai M., Alboresi A., Burlacot A., Dautermann O., et al. (2021a). Role of an ancient light-harvesting protein of PSI in light absorption and photoprotection. PubMed DOI PMC

Lu Y., Jiang J., Zhao H., Han X., Xiang Y., Zhou W. (2020). Clade-specific sterol metabolites in dinoflagellate endosymbionts are associated with coral bleaching in response to environmental cues. PubMed DOI PMC

Lu Y., Jiang P., Liu S., Gan Q., Cui H., Qin S. (2010). Methyl jasmonate- or gibberellins A3-induced astaxanthin accumulation is associated with up-regulation of transcription of beta-carotene ketolase genes (bkts) in microalga Haematococcus pluvialis. PubMed DOI

Lu Y., Tarkowská D., Turečková V., Luo T., Xin Y., Li J., et al. (2014). Antagonistic roles of abscisic acid and cytokinin in oleaginous microalga Nannochloropsis oceanica upon nitrogen-depletion expand the evolutionary breadth of phytohormone function. PubMed DOI

Park W.-K., Yoo G., Moon M., Kim C. W., Choi Y.-E., Yang J.-W. (2013). Phytohormone supplementation significantly increases growth of Chlamydomonas reinhardtii cultivated for biodiesel production. PubMed DOI

Peleg Z., Blumwald E. (2011). Hormone balance and abiotic stress tolerance in crop plants. PubMed DOI

Piotrowska-Niczyporuk A., Bajguz A., Zambrzycka E., Godlewska-Żyłkiewicz B. (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). PubMed DOI

Piotrowskaniczyporuk A., Bajguz A., Zambrzycka E., Godlewska-Żylkiewicz B. (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). PubMed

Rensing S. A., Lang D., Zimmer A. D., Terry A., Salamov A., Shapiro H., et al. (2008). The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. PubMed DOI

Roth M. S. (2014). The engine of the reef: photobiology of the coral-algal symbiosis. PubMed DOI PMC

Shoguchi E., Shinzato C., Kawashima T., Gyoja F., Mungpakdee S., Koyanagi R. (2013). Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. PubMed DOI

Sponsel V. M., Hedden P. (2010). “Gibberellin biosynthesis and inactivation,” in

Stirk W. A., Bálint P., Tarkowská D., Novák O., Maróti G., Ljung K. (2014). Effect of light on growth and endogenous hormones in Chlorella minutissima (Trebouxiophyceae). PubMed DOI

Sun T. P., Kamiya Y. (1994). The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. PubMed DOI PMC

Tudzynski B., Kawaide H., Kamiya Y. (1998). Gibberellin biosynthesis in Gibberella fujikuroi: cloning and characterization of the copalyl diphosphate synthase gene. PubMed DOI

Urbanová T., Tarkowská D., Novák O., Hedden P., Strnad M. (2013). Analysis of gibberellins as free acids by ultra performance liquid chromatography–tandem mass spectrometry. PubMed DOI

Yamaguchi S., Sun T., Kawaide H., Kamiya Y. (1998). The GA2 locus of Arabidopsis thaliana encodes ent-Kaurene synthase of gibberellin biosynthesis. PubMed DOI PMC

Yasumura Y., Crumpton-Taylor M., Fuentes S., Harberd N. P. (2007). Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. PubMed DOI

Yu X. J., Sun J., Sun Y.-Q., Zheng J.-Y., Wang Z. (2016). Metabolomics analysis of phytohormone gibberellin improving lipid and DHA accumulation in Aurantiochytrium sp.

Zanewich K. P., Rood S. B. (1995). Vernalization and gibberellin physiology of winter canola (endogenous gibberellin (GA) content and metabolism of [3H]GA1 and [3H]GA20. PubMed DOI PMC

Zhou W., Zhang X., Wang A., Gan Q., Yang L., Yi L., et al. (2022). A widespread sterol methyl transferase participates in the biosynthesis of both C4α and C4β-methyl sterols. PubMed DOI PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...