Genome-Wide Characterization of Light-Regulated Genes in<i>Neurospora crassa</i>

Wu, Cheng; Yang, Fengtang; Smith, Kristina M.; Peterson, Michael; Dekhang, Rigzin; Zhang, Ying; Zucker, Jeremy; Bredeweg, Erin L.; Mallappa, Chandrashekara; Zhou, Xiaoying; Lyubetskaya, Anna; Townsend, Jeffrey P.; Galagan, James E.; Freitag, Michael; Dunlap, Jay C.; Bell-Pedersen, Deborah; Sachs, Matthew S.

doi:10.1534/g3.114.012617

Cited by 86 publications

(117 citation statements)

References 83 publications

(141 reference statements)

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“…For 237, the 39-UTR-intron was present in all predicted transcript models. We examined these 237 transcripts using our recently published RNA-seq data (Wu et al 2014). We obtained clear evidence for a spliced 39-UTR intron in 31 cases (Table S3).…”

Section: Discussionmentioning

confidence: 99%

“…The Neurospora crassa gene models from release 7 indicates 321 of the 9728 predicted protein coding genes in N. crassa potentially have 3'UTR introns. For 237, the 3'UTR-intron was present in all expected forms of the transcript were further examined according to our recently published RNA-seq data for wt (Wu et al 2014). 31 mRNAs with spliced 3'UTR introns were identified and their predicted 3'UTR and 3'UTR intron-lengths were calculated based on N. crassa RNA-seq data; additional information about these genes is also listed.…”

Section: Literature Citedmentioning

confidence: 99%

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Control of mRNA Stability in Fungi by NMD, EJC and CBC Factors Through 3′UTR Introns

Zhang¹,

Sachs

2015

Genetics

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In higher eukaryotes the accelerated degradation of mRNAs harboring premature termination codons is controlled by nonsense-mediated mRNA decay (NMD), exon junction complex (EJC), and nuclear cap-binding complex (CBC) factors, but the mechanistic basis for this quality-control system and the specific roles of the individual factors remain unclear. Using Neurospora crassa as a model system, we analyzed the mechanisms by which NMD is induced by spliced 39-UTR introns or upstream open reading frames and observed that the former requires NMD, EJC, and CBC factors whereas the latter requires only the NMD factors. The transcripts for EJC components eIF4A3 and Y14, and translation termination factor eRF1, contain spliced 39-UTR introns and each was stabilized in NMD, EJC, and CBC mutants. Reporter mRNAs containing spliced 39-UTR introns, but not matched intronless controls, were stabilized in these mutants and were enriched in mRNPs immunopurified from wild-type cells with antibody directed against human Y14, demonstrating a direct role for spliced 39-UTR introns in triggering EJC-mediated NMD. These results demonstrate conclusively that NMD, EJC, and CBC factors have essential roles in controlling mRNA stability and that, based on differential requirements for these factors, there are branched mechanisms for NMD. They demonstrate for the first time autoregulatory control of expression at the level of mRNA stability through the EJC/CBC branch of NMD for EJC core components, eIF4A3 and Y14, and for eRF1, which recognizes termination codons. Finally, these results show that EJC-mediated NMD occurs in fungi and thus is an evolutionarily conserved quality-control mechanism.KEYWORDS nonsense-mediated mRNA decay (NMD); RNA stability; exon junction complex (EJC); cap-binding complex (CBC); spliced 39-UTR intron; post-transcriptional control; ribosome; translation; Neurospora crassa T HE nonsense-mediated mRNA decay (NMD) pathway targets mRNA for degradation through the recognition of translated termination codons determined to be premature (Nicholson et al. 2009;Kervestin and Jacobson 2012;Popp and Maquat 2013). The NMD pathway can degrade mRNAs that contain upstream open reading frames (uORFs) or long 39-UTRs. The termination-related processes that trigger uORFmediated or long 39-UTR-mediated NMD are considered to be similar (Amrani et al. 2004(Amrani et al. , 2006Nicholson et al. 2009) in that termination events occurring far from the context created by the mRNA poly(A) tail can result in mRNA degradation (the "faux-UTR" model). In higher eukaryotes, NMD can also act on mRNAs that contain an intron downstream of a termination codon, such as aberrantly spliced transcripts or 39-UTR introncontaining transcripts (Sauliere et al. 2010;Bicknell et al. 2012). When a spliced intron is positioned at least 50-55 nt downstream of a termination codon, the exon junction complex (EJC) positioned near the exon-exon junction is not displaced by translating ribosomes and its continued association with mRNA targets the mRNA for deg...

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Section: Discussionmentioning

confidence: 99%

Section: Literature Citedmentioning

confidence: 99%

Control of mRNA Stability in Fungi by NMD, EJC and CBC Factors Through 3′UTR Introns

Zhang¹,

Sachs

2015

Genetics

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“…H 2 O 2 (0.5 to 1 mM), besides light, activates the white collar complex; transcribes the cat-1 gene, the main catalase of conidiation (331); and generates a cat-1 mRNA cycle (332). Consistent with the role of ROS in cyclic conidiation, many light-induced genes in N. crassa encode antioxidants (333).…”

Section: Transitions From Vegetative Growth To Asexual Developmentmentioning

confidence: 99%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

273

246

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SUMMARYFilamentous fungi constitute a large group of eukaryotic microorganisms that grow by forming simple tube-like hyphae that are capable of differentiating into more-complex morphological structures and distinct cell types. Hyphae form filamentous networks by extending at their tips while branching in subapical regions. Rapid tip elongation requires massive membrane insertion and extension of the rigid chitin-containing cell wall. This process is sustained by a continuous flow of secretory vesicles that depends on the coordinated action of the microtubule and actin cytoskeletons and the corresponding motors and associated proteins. Vesicles transport cell wall-synthesizing enzymes and accumulate in a special structure, the Spitzenkörper, before traveling further and fusing with the tip membrane. The place of vesicle fusion and growth direction are enabled and defined by the position of the Spitzenkörper, the so-called cell end markers, and other proteins involved in the exocytic process. Also important for tip extension is membrane recycling by endocytosis via early endosomes, which function as multipurpose transport vehicles for mRNA, septins, ribosomes, and peroxisomes. Cell integrity, hyphal branching, and morphogenesis are all processes that are largely dependent on vesicle and cytoskeleton dynamics. When hyphae differentiate structures for asexual or sexual reproduction or to mediate interspecies interactions, the hyphal basic cellular machinery may be reprogrammed through the synthesis of new proteins and/or the modification of protein activity. Although some transcriptional networks involved in such reprogramming of hyphae are well studied in several model filamentous fungi, clear connections between these networks and known determinants of hyphal morphogenesis are yet to be established.

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“…The fraction of genes identified as light-induced has ranged widely (3%–31%) in various studies primarily due to differences in methodology (microarrays vs. RNA-seq), culture conditions, and fold-change cut-offs imposed (Lewis et al , 2002; Dong et al , 2008; Chen et al , 2009; Wu et al , 2014), with RNA-Seq, the most quantitative and sensitive technology (Wang et al , 2009; Zhao et al , 2014), revealing that nearly 31% of expressed genes show two-fold or more change when N. crassa is exposed to light (Wu et al , 2014). Unique to this study was the finding that a subset of mRNAs was actually significantly down-regulated in response to light exposure (e.g.…”

Section: N Crassa: a Model Organism For Studying Photobiologymentioning

confidence: 99%

Seeing the world differently: variability in the photosensory mechanisms of two model fungi

Dasgupta

Fuller

Dunlap

et al. 2015

Environmental Microbiology

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Summary Light plays an important role for most organisms on this planet, serving either as a source of energy or information for the adaptation of biological processes to specific times of day. The fungal kingdom is estimated to contain well over a million species, possibly ten-fold more, and it is estimated that a majority of the fungi respond to light, eliciting changes in several physiological characteristics including pathogenesis, development and secondary metabolism. Two model organisms for photobiological studies have taken center-stage over the last few decades – Neurospora crassa and Aspergillus nidulans. In this review, we will first discuss our understanding of the light response in N. crassa, about which the most is known, and will then juxtapose N. crassa with A. nidulans which, as will be described below, provides an excellent template for understanding photosensory cross-talk. Finally, we will end with a commentary on the variability of the light response among other relevant fungi, and how our molecular understanding in the aforementioned model organisms still provides a strong base for dissecting light responses in such species.

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Genome-Wide Characterization of Light-Regulated Genes inNeurospora crassa

Cited by 86 publications

References 83 publications

Control of mRNA Stability in Fungi by NMD, EJC and CBC Factors Through 3′UTR Introns

Control of mRNA Stability in Fungi by NMD, EJC and CBC Factors Through 3′UTR Introns

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Seeing the world differently: variability in the photosensory mechanisms of two model fungi

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