Plants deploy cell-surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding site–leucine-rich repeat receptors (NLRs) to recognize pathogens. However, how plant immune receptor repertoires evolve in responding to changed pathogen burdens remains elusive. Here we reveal the convergent reduction of NLR repertoires in plants with diverse special lifestyles/habitats (SLHs) encountering low pathogen burdens. Furthermore, a parallel but milder reduction of PRR genes in SLH species was observed. The reduction of PRR and NLR genes was attributed to both increased gene loss and decreased gene duplication. Notably, pronounced loss of immune receptors was associated with the complete absence of signalling components from the enhanced disease susceptibility 1 (EDS1) and the resistance to powdery mildew 8 (RPW8)-NLR (RNL) families. In addition, evolutionary pattern analysis suggested that the conserved toll/interleukin-1 receptor (TIR)-only proteins might function tightly with EDS1/RNL. Taken together, these results reveal the hierarchically adaptive evolution of the two-tiered immune receptor repertoires during plant adaptation to diverse SLHs.
N6-Methyladenosine (m6A) is the most widespread modification of mRNA and is required to control mRNA stability and translation efficiency. In plants, its effect is mediated by m6A reader proteins such as EVOLUTIONARILY CONSERVED C-TERMINAL REGION (ECT) proteins. Marlene Reichel from the University of Copenhagen, and colleagues, find that the m6A binding and reader function of ECT2 in Arabidopsis requires proteins from the ACETYLATION LOWERS BINDING AFFINITY (ALBA) family, which suggests that these factors form an m6A reader complex.
Arabidopsis encodes eleven ECTs; of these, ECT2 and ECT3 have the most important role in post-embryonic development, and ECT4 has a more minor contribution. The ect2 ect3 ect4 (ect2/3/4) triple mutants display delayed organogenesis and aberrant morphology, including misshaped leaves, petals and siliques as well as increased trichome branching. These ECTs bind to m6A modifications in the 3′ untranslated region of mRNAs and recruit poly(A) binding proteins to enhance mRNA stability. However, the exact mode of mRNA binding of ECTs and whether other factors are involved was unclear.
Parthenocarpy is a pivotal trait that enhances the yield and quality of fruit crops by enabling the development of seedless fruits. Here we unveil a molecular framework for the regulation and domestication of parthenocarpy in cucumber (Cucumis sativus L.). We previously discovered a natural non-parthenocarpic mutant and demonstrated that the AP2-like transcription factor NON-PARTHENOCARPIC FRUIT 1 (NPF1) is a central regulator of parthenocarpy through activating YUC4 expression and promoting auxin biosynthesis in ovules. A Phe-to-Ser substitution at amino acid residue 7 results in a stable form of NPF1 that is localized in the nucleus. An A-to-G polymorphism (SNP-383) within an NPF1-binding site in the YUC4 promoter significantly enhances the activation of NPF1 towards YUC4, leading to an increased rate of parthenocarpy. Additionally, NPF1 influences bitterness by reducing cucurbitacin C biosynthesis through the suppression of Bt expression. Our results suggest a two-step evolutionary model for parthenocarpy and fruit bitterness during cucumber domestication.
Precise manipulation of genome structural variations holds great potential for plant trait improvement and biological research. Here we present a genome-editing approach, dual prime editing (DualPE), that efficiently facilitates precise deletion, replacement and inversion of large DNA fragments in plants. In our experiments, DualPE enabled the production of specific genomic deletions ranging from ~500 bp to 2 Mb in wheat protoplasts and plants. DualPE was effective in directly replacing wheat genomic fragments of up to 258 kb with desired sequences in the absence of donor DNA. Additionally, DualPE allowed precise DNA inversions of up to 205.4 kb in wheat plants with efficiencies of up to 51.5%. DualPE also successfully edited large DNA fragments in the dicots Nicotiana benthamiana and tomato, with editing efficiencies of up to 72.7%. DualPE thus provides a precise and efficient approach for large DNA sequence and chromosomal engineering, expanding the availability of precision genome-editing tools for crop improvement.
Hydrogen peroxide (H2O2) functions as a critical signalling molecule in controlling multiple biological processes. How H2O2 signalling integrates with other regulatory pathways such as epigenetic modification to coordinately regulate plant development remains elusive. Here we report that SlALKBH2, an m6A demethylase required for normal ripening of tomato fruit, is sensitive to oxidative modification by H2O2, which leads to the formation of homodimers mediated by intermolecular disulfide bonds, and Cys39 serves as a key site in this process. The oxidation of SlALKBH2 promotes protein stability and facilitates its function towards the target transcripts including the pivotal ripening gene SlDML2 encoding a DNA demethylase. Furthermore, we demonstrate that the thioredoxin reductase SlNTRC interacts with SlALKBH2 and catalyses its reduction, thereby modulating m6A levels and fruit ripening. Our study establishes a molecular link between H2O2 and m6A methylation and highlights the importance of redox regulation of m6A modifiers in controlling fruit ripening.
Orchids constitute one of the most diverse families of angiosperms, yet their genome evolution and diversity remain unclear. Here we construct and analyse chromosome-scale de novo assembled genomes of 17 representative accessions spanning 12 sections in Dendrobium, one of the largest orchid genera. These accessions represent a broad spectrum of phenotypes, lineages and geographical distributions. We first construct haplotype-resolved genomes for a Dendrobium hybrid and uncover haplotypic variations and allelic imbalance in the heterozygous genome, demonstrating the significance of diverse ancestry. At Dendrobium genus-wide scale, we further elucidate phylogenetic relationships, evolutionary dynamics, entire gene repertoire, and the mechanisms of preserving ancient genetic variants and rapid recent genome evolution for habitat adaption. We also showcase distinctive evolutionary trajectories in MADS-box and PEBP families over 28 Ma. These results considerably contribute to unearthing the mystery of orchid origin, evolution and diversification, laying the foundation for efficient use of genetic diversity in breeding.
Pseudouridine (Ψ) is the most abundant RNA modification, yet studies of Ψ have been hindered by a lack of robust methods to profile comprehensive Ψ maps. Here we utilize bisulfite-induced deletion sequencing to generate transcriptome-wide Ψ maps at single-base resolution across various plant species. Integrating ribosomal RNA, transfer RNA and messenger RNA Ψ stoichiometry with mRNA abundance and polysome profiling data, we uncover a multilayered regulation of translation efficiency through Ψ modifications. rRNA pseudouridylation could globally control translation, although the effects vary at different rRNA Ψ sites. Ψ in the tRNA T-arm loop shows strong positive correlations between Ψ stoichiometry and the translation efficiency of their respective codons. We observed a general inverse correlation between Ψ level and mRNA stability, but a positive correlation with translation efficiency in Arabidopsis seedlings. In conclusion, our study provides critical resources for Ψ research in plants and proposes prevalent translation regulation through rRNA, tRNA and mRNA pseudouridylation.