Plant evolution is driven by key innovations of functional traits that enables their survivals in diverse ecological environments. However, plant adaptive evolution from land to atmospheric niches remains poorly understood. In this study, we use the epiphytic Tillandsioideae subfamily of Bromeliaceae as model plants to explore their origin, evolution and diversification. We provide a comprehensive phylogenetic tree based on nuclear transcriptomic sequences, indicating that core tillandsioids originated approximately 11.3 million years ago in the Andes. The geological uplift of the Andes drives the divergence of tillandsioids into tank-forming and atmospheric types. Our genomic and transcriptomic analyses reveal gene variations and losses associated with adaptive traits such as impounding tanks and absorptive trichomes. Furthermore, we uncover specific nitrogen-fixing bacterial communities in the phyllosphere of tillandsioids as potential source of nitrogen acquisition. Collectively, our study provides integrative multi-omics insights into the adaptive evolution of tillandsioids in response to elevated aerial habitats.

Summary: Eukaryotic translation initiation factors (eIFs) are the primary targets for overcoming RNA virus resistance in plants. In a previous study, we mapped a BjeIF2Bβ from Brassica juncea representing a new class of plant virus resistance genes associated with resistance to Turnip mosaic virus (TuMV). However, the mechanism underlying eIF2Bβ‐mediated virus resistance remains unclear. In this study, we discovered that the natural variation of BjeIF2Bβ in the allopolyploid B. juncea was inherited from one of its ancestors, B. rapa. By editing of eIF2Bβ, we were able to confer resistance to TuMV in B. juncea and in its sister species of B. napus. Additionally, we identified an N⁶‐methyladenosine (m⁶A) demethylation factor, BjALKBH9B, for interaction with BjeIF2Bβ, where BjALKBH9B co‐localized with both BjeIF2Bβ and TuMV. Furthermore, BjeIF2Bβ recruits BjALKBH9B to modify the m⁶A status of TuMV viral coat protein RNA, which lacks the ALKB homologue in its genomic RNA, thereby affecting viral infection. Our findings have applications for improving virus resistance in the Brassicaceae family through natural variation or genome editing of the eIF2Bβ. Moreover, we uncovered a non‐canonical translational control of viral mRNA in the host plant.

Non-Mendelian transmission of mitochondria has been well established across most eukaryotes, however the genetic mechanism that governs this uniparental inheritance remains unclear. Plants in the genus Cucumis, specifically melon and cucumber, exhibit paternal transmission of the mitochondrial (mt) DNA, making them excellent models for exploring the molecular mechanisms underlying mitochondrial transmission. Here, we develop a toolkit to screen for mutants in mitochondrial inheritance (mti), and use fine mapping to successfully identify a mitochondrially targeted endonuclease gene (MTI1) controlling mitochondrial transmission. Knockout of MTI1 results in a shift from paternal to bi-parental inheritance of the mtDNA, confirming the crucial role of MTI1 in uniparental inheritance of mitochondria. Moreover, we demonstrate that MTI1 exhibits robust endonuclease activity both in vitro and in vivo, specifically expresses in mitochondria of the fertilized ovule within 24 h of pollination. Collectively, this study reveals that a nuclear-encoded but mitochondria-targeted gene plays a causative role in governing the non-Mendelian mitochondrial inheritance, revolutionizing our knowledge about mitochondrial DNA transmission.

Summary: Global climate change has rendered drought stress an increasing threat to sustainable crop production. Melon (Cucumis melo) crop is widely cultivated worldwide, and has been classified into two subspecies C. melo ssp. melo and C. melo ssp. agrestis with greater drought tolerance variation. However, the genetic basis for the difference in drought resilience between two subspecies ecotypes remains unclear. In this study, we constructed an F₈ recombinant inbred lines (RILs) population generated by crossing drought‐tolerant C. melo ssp. melo with drought‐sensitive C. melo ssp. agrestis and identified a CmPPR4 gene that encoded a pentatricopeptide repeat (PPR) protein highly associated with drought tolerance. A single nucleotide polymorphism (SNP) variation in CmPPR4 resulted in a nonsynonymous mutation, leading to reduced drought resilience in C. melo ssp. agrestis. The geographical distribution of CmPPR4 genotypes among 297 melon accessions closely parallels global annual precipitation patterns. Furthermore, the diminished drought tolerant capacity in RNA silencing seedlings and enhanced drought tolerance in overexpression lines further confirmed CmPPR4 as a crucial regulator of drought tolerance in melon. Collectively, our findings provide new insights into the crucial role of CmPPR4 in regulating drought tolerance of melon ecotypes, promoting molecular breeding of water‐saving and drought‐resilient melon cultivars.

Fruit length (FL) is an important economical trait that affects fruit yield and appearance. Pumpkin (Cucurbita moschata Duch) contains a wealth genetic variation in fruit length. However, the natural variation underlying differences in pumpkin fruit length remains unclear. In this study, we constructed a F₂ segregate population using KG1 producing long fruit and MBF producing short fruit as parents to identify the candidate gene for fruit length. By bulked segregant analysis (BSA-seq) and Kompetitive Allele-Specific PCR (KASP) approach of fine mapping, we obtained a 50.77 kb candidate region on chromosome 14 associated with the fruit length. Then, based on sequence variation, gene expression and promoter activity analyses, we identified a candidate gene (CmoFL1) encoding E3 ubiquitin ligase in this region may account for the variation of fruit length. One SNP variation in promoter of CmoFL1 changed the GT1CONSENSUS, and DUAL-LUC assay revealed that this variation significantly affected the promoter activity of CmoFL1. RNA-seq analysis indicated that CmoFL1 might associated with the cell division process and negatively regulate fruit length. Collectively, our work identifies an important allelic affecting fruit length, and provides a target gene manipulating fruit length in future pumpkin breeding.