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N6-Methyladenosine (m6A) RNA methylation plays important roles during development in different species. However, knowledge of m6A RNA methylation in monocots remains limited. In this study, we reported that OsFIP and OsMTA2 are the components of m6A RNA methyltransferase complex in rice and uncovered a previously unknown function of m6A RNA methylation in regulation of plant sporogenesis. Importantly, OsFIP is essential for rice male gametogenesis. Knocking out of OsFIP results in early degeneration of microspores at the vacuolated pollen stage and simultaneously causes abnormal meiosis in prophase I. We further analyzed the profile of rice m6A modification during sporogenesis in both WT and OsFIP loss-of-function plants, and identified a rice panicle specific m6A modification motif \"UGWAMH\". Interestingly, we found that OsFIP directly mediates the m6A methylation of a set of threonine protease and NTPase mRNAs and is essential for their expression and/or splicing, which in turn regulates the progress of sporogenesis. Our findings revealed for the first time that OsFIP plays an indispensable role in plant early sporogenesis. This study also provides evidence for the different functions of the m6A RNA methyltransferase complex between rice and Arabidopsis.

Because their resistant, sporopolleninous walls preserve a record of morphogenetic change during spore formation, fossil cryptospores provide a direct physical record of the evolution of sporogenesis during the algal–plant transition. That transition itself is a story of the evolution of development—it is not about phylogeny. Here, we review the fossil record of terrestrially derived spore/cryptospore assemblages and attempt to place these microfossils in their evolutionary context with respect to the origin of complex multicellularity in plants. Cambrian cryptospores show features related to karyokinesis seen in extant charophytes, but they also possess ultrastructure similar to that seen in liverworts today. Dyadospora, a cryptospore dyad recovered from sporangia of Devonian embryophytes, first occurs in the earliest Ordovician. Tetrahedraletes, a likely precursor to the trilete spore, first occurs in the Middle Ordovician. These fossils correspond to evolutionary novelties that were acquired during a period of genome assembly prior to the existence of upright, axial sporophytes. The cryptospore/spore fossil record provides a temporal scaffold for the acquisition of novel characters relating to the evolution of plant sporogenesis during the Cambrian–Silurian interval.

In angiosperms, the key step in sexual reproduction is successful acquisition of meiotic fate. However, the molecular mechanism determining meiotic fate remains largely unknown. Here, we report that OsSPOROCYTELESS (OsSPL) is critical for meiotic entry in rice (Oryza sativa). We performed a large-scale genetic screen of rice sterile mutants aimed to identify genes regulating meiotic entry and identified OsSPL using map-based cloning. We showed that meiosis-specific callose deposition, chromatin organization, and centromere-specific histone H3 loading were altered in the cells corresponding to pollen mother cells in Osspl anthers. Global transcriptome analysis showed that the enriched differentially expressed genes in Osspl were mainly related to redox status, meiotic process, and parietal cell development. OsSPL might form homodimers and interact with TEOSINTE BRANCHED1/CYCLOIDEA/PCF (TCP) transcription factor OsTCP5 via the SPL dimerization and TCP interaction domain. OsSPL also interacts with TPL (TOPLESS) corepressors, OsTPL2 and OsTPL3, via the EAR motif. Our results suggest that the OsSPL-mediated signaling pathway plays a crucial role in rice meiotic entry, which appears to be a conserved regulatory mechanism for meiotic fate acquisition in angiosperms.

The conidia produced by Fusarium oxysporum f. sp. cubense (Foc), the causative agent of Fusarium Wilt of Banana (FWB), play central roles in the disease cycle, as the pathogen lacks a sexual reproduction process. Until now, the molecular regulation network of asexual sporogenesis has not been clearly understood in Foc. Herein, we identified and functionally characterized thirteen (13) putative sporulation-responsive genes in Foc, namely FocmedA(a), FocmedA(b), abaA-L, FocflbA, FocflbB, FocflbC, FocflbD, FocstuA, FocveA, FocvelB, wetA-L, FocfluG and Foclae1. We demonstrated that FocmedA(a), abaA-L, wetA-L, FocflbA, FocflbD, FocstuA, FocveA and Foclae1 mediate conidiophore formation, whereas FocmedA(a) and abaA-L are important for phialide formation and conidiophore formation. The expression level of abaA-L was significantly decreased in the ΔFocmedA(a) mutant, and yeast one-hybrid and ChIP-qPCR analyses further confirmed that FocMedA(a) could bind to the promoter of abaA-L during micro- and macroconidiation. Moreover, the transcript abundance of the wetA-L gene was significantly reduced in the ΔabaA-L mutant, and it not only was found to function as an activator of micro- and macroconidium formation but also served as a repressor of chlamydospore production. In addition, the deletions of FocflbB, FocflbC, FocstuA and Foclae1 resulted in increased chlamydosporulation, whereas FocflbD and FocvelB gene deletions reduced chlamydosporulation. Furthermore, FocflbC, FocflbD, Foclae1 and FocmedA(a) were found to be important regulators for pathogenicity and fusaric acid synthesis in Foc. The present study therefore advances our understanding of the regulation pathways of the asexual development and functional interdependence of sporulation-responsive genes in Foc.

• Algal viruses are important contributors to carbon cycling, recycling nutrients and organic material through host lysis. Although viral infection has been described as a primary mechanism of phytoplankton mortality, little is known about host defense responses. • We show that viral infection of the bloom-forming, planktonic diatom Chaetoceros socialis induces the mass formation of resting spores, a heavily silicified life cycle stage associated with carbon export due to rapid sinking. • Although viral RNA was detected within spores, mature virions were not observed. ‘Infected’ spores were capable of germinating, but did not propagate or transmit infectious viruses. • These results demonstrate that diatom spore formation is an effective defense strategy against viral-mediated mortality. They provide a possible mechanistic link between viral infection, bloom termination, and mass carbon export events and highlight an unappreciated role of viruses in regulating diatom life cycle transitions and ecological success.

• The biotrophic basidiomycete fungus Ustilago maydis causes smut disease in maize. Hallmarks of the disease are characteristic large tumors in which dark pigmented spores are formed. Here, we functionally characterized a novel core effector lep1 (late effector protein 1) which is highly expressed during tumor formation and contributes to virulence. • We characterize lep1 mutants, localize the protein, determine phenotypic consequences upon deletion as well as constitutive expression, and analyze relationships with the repellent protein Rep1 and hydrophobins. • In tumors, lep1 mutants show attenuated hyphal aggregation, fail to undergo massive late proliferation and produce only a few spores. Upon constitutive expression, cell aggregation is induced and the surface of filamentous colonies displays enhanced hydrophobicity. Lep1 is bound to the cell wall of biotrophic hyphae and associates with Rep1 when constitutively expressed in hyphae. • We conclude that Lep1 acts as a novel kind of cell adhesin which functions together with other surface-active proteins to allow proliferation of diploid hyphae as well as for induction of the morphological changes associated with spore formation.

A wox1 mutant cucumber plant with sterile male and female flowers suggests that CsWOX1 regulates early reproductive organ development and may be involved in sporogenesis via the CsSPL-mediated pathway. Abstract The WUSCHEL-related homeobox1 (WOX1) transcription factor plays an important role in lateral growth of plant organs; however, the underlying mechanisms in the regulation of reproductive development are largely unknown. Cucumber (Cucumis sativus) has separate male and female flowers, facilitating the study of the role of WOX1 in stamen and carpel development. Here, we identified a mango fruit (mf) mutant in cucumber, which displayed multiple defects in flower growth as well as male and female sterility. Map-based cloning showed that Mf encodes a WOX1-type transcriptional regulator (CsWOX1), and that the mf mutant encodes a truncated protein lacking the conserved WUS box. Further analysis showed that elevated expression of CsWOX1 was responsible for the mutant phenotype in cucumber and Arabidopsis. Comparative transcriptome profiling revealed certain key players and CsWOX1-associated networks that regulate reproductive development. CsWOX1 directly interacts with cucumber SPOROCYTELESS (CsSPL), and many genes in the CsSPL-mediated pathway were down-regulated in plants with the mutant allele at the Mf locus. In addition, auxin distribution was affected in both male and female flowers of the mutant. Taking together, these data suggest that CsWOX1 may regulate early reproductive organ development and be involved in sporogenesis via the CsSPL-mediated pathway and/or modulate auxin signaling in cucumber.

Sorghum [Sorghum bicolor (L.) Moench] yield formation is severely affected by high temperature stress during reproductive stages. This study pursues to (i) identify the growth stage(s) most sensitive to high temperature stress during reproductive development, (ii) determine threshold temperature and duration of high temperature stress that decreases floret fertility and individual grain weight, and (iii) quantify impact of high daytime temperature during floret development, flowering and grain filling on reproductive traits and grain yield under field conditions. Periods between 10 and 5 d before anthesis; and between 5 d before- and 5 d after-anthesis were most sensitive to high temperatures causing maximum decreases in floret fertility. Mean daily temperatures >25°C quadratically decreased floret fertility (reaching 0% at 37°C) when imposed at the start of panicle emergence. Temperatures ranging from 25 to 37°C quadratically decreased individual grain weight when imposed at the start of grain filling. Both floret fertility and individual grain weights decreased quadratically with increasing duration (0-35 d or 49 d during floret development or grain filling stage, respectively) of high temperature stress. In field conditions, imposition of temperature stress (using heat tents) during floret development or grain filling stage also decreased floret fertility, individual grain weight, and grain weight per panicle.

Filamentous fungi produce a vast number of asexual spores that act as efficient propagules. Due to their infectious and/or allergenic nature, fungal spores affect our daily life. Aspergillus species produce asexual spores called conidia; their formation involves morphological development and metabolic changes, and the associated regulatory systems are coordinated by multiple transcription factors (TFs). In filamentous fungi, asexual development involves cellular differentiation and metabolic remodeling leading to the formation of intact asexual spores. The development of asexual spores (conidia) in Aspergillus is precisely coordinated by multiple transcription factors (TFs), including VosA, VelB, and WetA. Notably, these three TFs are essential for the structural and metabolic integrity, i.e., proper maturation, of conidia in the model fungus Aspergillus nidulans . To gain mechanistic insight into the complex regulatory and interdependent roles of these TFs in asexual sporogenesis, we carried out multi-omics studies on the transcriptome, protein-DNA interactions, and primary and secondary metabolism employing A. nidulans conidia. RNA sequencing and chromatin immunoprecipitation sequencing analyses have revealed that the three TFs directly or indirectly regulate the expression of genes associated with heterotrimeric G-protein signal transduction, mitogen-activated protein (MAP) kinases, spore wall formation and structural integrity, asexual development, and primary/secondary metabolism. In addition, metabolomics analyses of wild-type and individual mutant conidia indicate that these three TFs regulate a diverse array of primary metabolites, including those in the tricarboxylic acid (TCA) cycle, certain amino acids, and trehalose, and secondary metabolites such as sterigmatocystin, emericellamide, austinol, and dehydroaustinol. In summary, WetA, VosA, and VelB play interdependent, overlapping, and distinct roles in governing morphological development and primary/secondary metabolic remodeling in Aspergillus conidia, leading to the production of vital conidia suitable for fungal proliferation and dissemination. IMPORTANCE Filamentous fungi produce a vast number of asexual spores that act as efficient propagules. Due to their infectious and/or allergenic nature, fungal spores affect our daily life. Aspergillus species produce asexual spores called conidia; their formation involves morphological development and metabolic changes, and the associated regulatory systems are coordinated by multiple transcription factors (TFs). To understand the underlying global regulatory programs and cellular outcomes associated with conidium formation, genomic and metabolomic analyses were performed in the model fungus Aspergillus nidulans . Our results show that the fungus-specific WetA/VosA/VelB TFs govern the coordination of morphological and chemical developments during sporogenesis. The results of this study provide insights into the interdependent, overlapping, or distinct genetic regulatory networks necessary to produce intact asexual spores. The findings are relevant for other Aspergillus species such as the major human pathogen Aspergillus fumigatus and the aflatoxin producer Aspergillus flavus .

Treatment with β-lactam antibiotics, particularly cephalosporins, is a major risk factor for Clostridioides difficile infection. These broad-spectrum antibiotics irreversibly inhibit penicillin-binding proteins (PBPs), which are serine-based enzymes that assemble the bacterial cell wall. However, C. difficile has four different PBPs (PBP1-3 and SpoVD) with various roles in growth and spore formation, and their specific links to β-lactam resistance in this pathogen are underexplored. Here, we show that PBP2 (known to be essential for vegetative growth) is the primary bactericidal target for β-lactams in C. difficile . PBP2 is insensitive to cephalosporin inhibition, and this appears to be the main basis for cephalosporin resistance in this organism. We determine crystal structures of C. difficile PBP2, alone and in complex with β-lactams, revealing unique features including ligand-induced conformational changes and an active site Zn 2+ -binding motif that influences β-lactam binding and protein stability. The Zn 2+ -binding motif is also present in C. difficile PBP3 and SpoVD (which are known to be essential for sporulation), as well as in other bacterial taxa including species living in extreme environments and the human gut. We speculate that this thiol-containing motif and its cognate Zn 2+ might function as a redox sensor to regulate cell wall synthesis for survival in adverse or anaerobic environments. Antibiotics of the β-lactam class inhibit bacterial cell wall synthesis by targeting penicillin-binding proteins (PBPs). Here, Sacco et al. study the four PBPs present in the pathogen C. difficile , revealing unique structural features and shedding light on the mechanisms underlying β-lactam resistance in this organism.