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Impact of light intensity and quality on chromatophore and nuclear gene expression in Paulinella chromatophora, an amoeba with nascent photosynthetic organelles

Published on Apr 1, 2017in Plant Journal 5.73
· DOI :10.1111/tpj.13488
Ru Zhang7
Estimated H-index: 7
(CIS: Carnegie Institution for Science),
Eva C. M. Nowack12
Estimated H-index: 12
(HHU: University of Düsseldorf)
+ 2 AuthorsArthur R. Grossman82
Estimated H-index: 82
(CIS: Carnegie Institution for Science)
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Abstract
Summary Plastid evolution has been attributed to a single primary endosymbiotic event that occurred about 1.6 billion years ago (BYA) in which a cyanobacterium was engulfed and retained by a eukaryotic cell, although early steps in plastid integration are poorly understood. The photosynthetic amoeba Paulinella chromatophora represents a unique model for the study of plastid evolution because it contains cyanobacterium-derived photosynthetic organelles termed ‘chromatophores’ that originated relatively recently (0.09–0.14 BYA). The chromatophore genome is about a third the size of the genome of closely related cyanobacteria, but 10-fold larger than most plastid genomes. Several genes have been transferred from the chromatophore genome to the host nuclear genome through endosymbiotic gene transfer (EGT). Some EGT-derived proteins could be imported into chromatophores for function. Two photosynthesis-related genes (psaI and csos4A) are encoded by both the nuclear and chromatophore genomes, suggesting that EGT in Paulinella chromatophora is ongoing. Many EGT-derived genes encode proteins that function in photosynthesis and photoprotection, including an expanded family of high-light-inducible (ncHLI) proteins. Cyanobacterial hli genes are high-light induced and required for cell viability under excess light. We examined the impact of light on Paulinella chromatophora and found that this organism is light sensitive and lacks light-induced transcriptional regulation of chromatophore genes and most EGT-derived nuclear genes. However, several ncHLI genes have reestablished light-dependent regulation, which appears analogous to what is observed in cyanobacteria. We postulate that expansion of the ncHLI gene family and its regulation may reflect the light/oxidative stress experienced by Paulinella chromatophora as a consequence of the as yet incomplete integration of host and chromatophore metabolisms.
  • References (70)
  • Citations (2)
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References70
Newest
Eva C. M. Nowack12
Estimated H-index: 12
(HHU: University of Düsseldorf),
Dana C. Price19
Estimated H-index: 19
(RU: Rutgers University)
+ 3 AuthorsArthur R. Grossman82
Estimated H-index: 82
(CIS: Carnegie Institution for Science)
Abstract Plastids, the photosynthetic organelles, originated >1 billion y ago via the endosymbiosis of a cyanobacterium. The resulting proliferation of primary producers fundamentally changed global ecology. Endosymbiotic gene transfer (EGT) from the intracellular cyanobacterium to the nucleus is widely recognized as a critical factor in the evolution of photosynthetic eukaryotes. The contribution of horizontal gene transfers (HGTs) from other bacteria to plastid establishment remains more contr...
36 Citations Source Cite
Published on Mar 15, 2016
Luis Delaye17
Estimated H-index: 17
(CINVESTAV),
Cecilio Valadez-Cano1
Estimated H-index: 1
,
Bernardo Pérez-Zamorano2
Estimated H-index: 2
17 Citations Source Cite
Mark Heinnickel10
Estimated H-index: 10
(CIS: Carnegie Institution for Science),
Rick G. Kim3
Estimated H-index: 3
(Stanford University)
+ 4 AuthorsArthur R. Grossman82
Estimated H-index: 82
(CIS: Carnegie Institution for Science)
Next Section Abstract A Chlamydomonas reinhardtii mutant lacking CGL71, a thylakoid membrane protein previously shown to be involved in photosystem I (PSI) accumulation, exhibited photosensitivity and highly reduced abundance of PSI under photoheterotrophic conditions. Remarkably, the PSI content of this mutant declined to nearly undetectable levels under dark, oxic conditions, demonstrating that reduced PSI accumulation in the mutant is not strictly the result of photodamage. Furthermore, PSI r...
15 Citations Source Cite
Published on Dec 1, 2015in Plant Cell Reports 3.50
Xiaofei Zeng3
Estimated H-index: 3
(WHU: Wuhan University),
Neng Cheng2
Estimated H-index: 2
(WHU: Wuhan University)
+ 5 AuthorsZhongli Hu6
Estimated H-index: 6
(WHU: Wuhan University)
Key message Six MnSOD genes were isolated from five Miscanthus species. MgMnSOD1 functions in mitochondria and MgMnSOD1 seems to be the main MnSOD gene involved in stress response of M. × giganteus.
3 Citations Source Cite
Published on Aug 25, 2015in Investigative Ophthalmology & Visual Science 3.81
Jin Hyoung Park5
Estimated H-index: 5
(UOU: University of Ulsan),
Soon-Suk Kang7
Estimated H-index: 7
(UOU: University of Ulsan)
+ 1 AuthorsHungwon Tchah19
Estimated H-index: 19
(UOU: University of Ulsan)
PURPOSE. We evaluated the effects of N-acetylcysteine (NAC), which is known to inhibit reactive oxygen species (ROS)‐dependent apoptosis, on high glucose‐induced ROS, apoptosis, inflammation, and delayed-wounding closure in primary cultured human conjunctival epithelial cells (pHCECs), and the regulatory effects of cleaved caspase-3, BAX, nuclear factor jB (NF-jB), IL-6, and TNF-a on these processes. METHODS. High glucose‐induced ROS generation was measured using 2 0 ,7 0 -dichlorofluorescein di...
7 Citations Source Cite
Chuan Ku11
Estimated H-index: 11
(HHU: University of Düsseldorf),
Shijulal Nelson-Sathi10
Estimated H-index: 10
(HHU: University of Düsseldorf)
+ 3 AuthorsWilliam Martin79
Estimated H-index: 79
(HHU: University of Düsseldorf)
Endosymbiotic theory in eukaryotic-cell evolution rests upon a foundation of three cornerstone partners—the plastid (a cyanobacterium), the mitochondrion (a proteobacterium), and its host (an archaeon)—and carries a corollary that, over time, the majority of genes once present in the organelle genomes were relinquished to the chromosomes of the host (endosymbiotic gene transfer). However, notwithstanding eukaryote-specific gene inventions, single-gene phylogenies have never traced eukaryotic gen...
45 Citations Source Cite
Published on May 4, 2015in ChemBioChem 2.59
Ryan T. Cassell2
Estimated H-index: 2
(FIU: Florida International University),
Wei Chen2
Estimated H-index: 2
(FIU: Florida International University)
+ 2 AuthorsKathleen S. Rein6
Estimated H-index: 6
(FIU: Florida International University)
The brevetoxins are neurotoxins that are produced by the “Florida red tide” dinoflagellate Karenia brevis. They bind to and activate the voltage-gated sodium channels in higher organisms, specifically the Nav1.4 and Nav1.5 channel subtypes. However, the native physiological function that the brevetoxins perform for K. brevis is unknown. By using fluorescent and photoactivatable derivatives, brevetoxin was shown to localize to the chloroplast of K. brevis where it binds to the light-harvesting co...
10 Citations Source Cite
Published on Apr 1, 2015in Nature Chemical Biology 12.15
Hristina Staleva4
Estimated H-index: 4
,
Josef Komenda34
Estimated H-index: 34
+ 4 AuthorsRoman Sobotka22
Estimated H-index: 22
Light-harvesting complexes (LHCs) manage energy flux into photosynthesis and dissipate excess light energy. The demonstration of dissipative energy transfer from chlorophyll-a to β-carotene in cyanobacterial high light–inducible proteins provides a mechanistic model for similar processes in LHCs.
76 Citations Source Cite
Published on Mar 1, 2015in Journal of Molecular Biology 5.07
Yamuna Devi Paila19
Estimated H-index: 19
(UMass: University of Massachusetts Amherst),
Lynn G.L. Richardson11
Estimated H-index: 11
(UMass: University of Massachusetts Amherst),
Danny J. Schnell39
Estimated H-index: 39
(UMass: University of Massachusetts Amherst)
Abstract The translocons at the outer (TOC) and the inner (TIC) envelope membranes of chloroplasts mediate the targeting and import of several thousand nucleus-encoded preproteins that are required for organelle biogenesis and homeostasis. The cytosolic events in preprotein targeting remain largely unknown, although cytoplasmic chaperones have been proposed to facilitate delivery to the TOC complex. Preprotein recognition is mediated by the TOC GTPase receptors Toc159 and Toc34. The receptors co...
74 Citations Source Cite
Published on Jan 1, 2015in Molecular Biology and Evolution 14.80
Lam-Tung Nguyen2
Estimated H-index: 2
(Medical University of Vienna),
Heiko A. Schmidt15
Estimated H-index: 15
(Medical University of Vienna)
+ 1 AuthorsBui Quang Minh15
Estimated H-index: 15
(Medical University of Vienna)
Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbat...
1,485 Citations Source Cite
Cited By2
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Published on May 28, 2019in New Phytologist 7.30
R I Ponce-Toledo (Université Paris-Saclay), Purificación López-García46
Estimated H-index: 46
(Université Paris-Saclay),
David Moreira54
Estimated H-index: 54
(Université Paris-Saclay)
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Published on Sep 1, 2017in Current Biology 9.19
Anna Singer3
Estimated H-index: 3
(HHU: University of Düsseldorf),
Gereon Poschmann16
Estimated H-index: 16
(HHU: University of Düsseldorf)
+ 6 AuthorsEva C. M. Nowack12
Estimated H-index: 12
(HHU: University of Düsseldorf)
Summary The endosymbiotic acquisition of mitochondria and plastids more than 1 Ga ago profoundly impacted eukaryote evolution. At the heart of understanding organelle evolution is the re-arrangement of the endosymbiont proteome into a host-controlled organellar proteome. However, early stages in this process as well as the timing of events that underlie organelle integration remain poorly understood. The amoeba Paulinella chromatophora contains cyanobacterium-derived photosynthetic organelles, t...
17 Citations Source Cite
Published on Jun 1, 2017in Current Opinion in Plant Biology 7.51
Guillaume Allorent6
Estimated H-index: 6
(Commissariat à l'énergie atomique et aux énergies alternatives),
Dimitris Petroutsos17
Estimated H-index: 17
(Commissariat à l'énergie atomique et aux énergies alternatives)
In photosynthetic organisms, proteins in the light-harvesting complex (LHC) harvest light energy to fuel photosynthesis, whereas photoreceptor proteins are activated by the different wavelengths of the light spectrum to regulate cellular functions. Under conditions of excess light, blue-light photoreceptors activate chloroplast avoidance movements in sessile plants, and blue- and green-light photoreceptors cause motile algae to swim away from intense light. Simultaneously, LHCs switch from light...
12 Citations Source Cite