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The evolutionary trajectories and gene regulatory roles of nuclear-integrated plastid DNA: clues for enhancing environmental adaptation in Caryophyllales.

Environmental stimuli can induce the transfer of chloroplast DNA to the nuclear genome, resulting in nuclear-integrated plastid DNAs (NUPTs). However, their role in plant adaptability remains unclear. Species within the Caryophyllales order, known for their adaptation to extreme environments, provide an ideal model for studying the evolutionary dynamics and functions of NUPTs. In this study, we analyzed NUPTs in 24 Caryophyllales species to investigate their evolution and regulatory roles in gene expression, particularly in response to environmental stimuli. We found significant interspecies variation in NUPT abundance, ranging from 566 insertions in Amaranthus cruentus to 3585 in Beta vulgaris, with sizes spanning from 100 bp to over 100 kb. Approximately 62% of NUPTs were inserted within the last 20 million years, while some species exhibit insertion peaks dating back 49 million years. NUPT presence/absence polymorphisms in six related species suggest that NUPT insertions and deletions are dynamic processes influenced by phylogeny. NUPTs predominantly integrate into intergenic regions but also insert into genes and promoters, with certain regions acting as hotspots. Notably, NUPTs introduce numerous environmental-responsive cis-acting elements in promoter regions. Genes with NUPT insertions in their promoters are significantly enriched for functions related to environmental response. Further luciferase assays in Spinacia oleracea demonstrated that NUPT insertions can regulate the expression of genes related to environmental responses, indicating their potential role in adaptive evolution. Overall, our study provides insights into NUPT evolution and their influence on gene function and plant adaptability to environmental stimuli.

Plastids

The genome sequence of Greek sea-spurrey, Spergularia bocconei (Scheele) Graebn. (Caryophyllaceae).

We present a genome assembly from a specimen of Spergularia bocconei (Greek sea-spurrey; Streptophyta; Magnoliopsida; Caryophyllales; Caryophyllaceae). The genome sequence has a total length of 466.20 megabases. Most of the assembly is scaffolded into 18 chromosomal pseudomolecules suggesting the individual is an allotetraploid (2 n = 4 x = 36). The mitochondrial and plastid genome assemblies have lengths of 327.07 kilobases and 152.41 kilobases, respectively.

Boccone's sea-spurrey

Characterization of culturable endophytes and microbial communities in the rhizosphere and pitcher fluid of the carnivorous plant Nepenthes khasiana.

Endophytes colonize plant tissues through roots and shoots without causing harm and can move throughout the plant via its vascular system. However, little is known about culturable endophytes, particularly bacteria, in pitcher plants, and their possible entry through pitcher fluid remains unexplored. To address this gap, we isolated endophytes from the pitcher plant Nepenthes khasiana, and performed metagenomic analysis of its rhizospheric soil and pitcher fluid, from which bacteria and fungi were also isolated, to investigate the possible origin of these endophytes. We found that culturable endophytic bacteria were predominantly associated with roots and seeds, whereas endophytic fungi were more abundant across the N. khasiana pitcher. Although most endophytes were restricted to specific tissues, some exhibited a broader distribution across nearly the entire plant. Several OTUs from the rhizospheric soil matched endophytes at the genus level, including some that were also detected in the pitcher fluid. Specifically, three bacterial genera - Enterobacter, Staphylococcus and Bacillus - and one fungal genus, Cladosporium, detected in the pitcher fluid, matched the isolated endophytes. These findings suggest that endophytes in N. khasiana most likely originate from the rhizosphere, with possible migration into the pitcher fluid.

Rhizosphere

The genome of Thesium ramosoides (Santalales) reveals evolutionary dynamics associated with parasitism and alpine adaptation.

Plant species adapting to complex environments experience contrasting selection pressures that drive the expansion and contraction of different gene families. However, few studies have investigated simultaneous genomic responses to such diverse selective forces. Here, we generate a high-quality genome assembly for the hemiparasitic plant Thesium ramosoides, the first for the largest genus in the Santalales, and explore the genomic basis underlying the evolution of parasitism and alpine adaptation. Unlike many other parasitic plants, the Thesium genome has not undergone additional rounds of whole-genome duplication, making it particularly tractable for studying gene family evolution. Our analyses reveal substantial loss of photosynthesis-related genes and contraction of biotic defense gene families, likely reflecting adaptation to a hemiparasitic lifestyle and reduced pathogen pressure at high altitudes. The absence of key root hair development genes correlates with the degenerate root hair phenotype observed in this species. Furthermore, hallmarks of high-altitude adaptation include the expansion of gene families involved in responses to hypoxia. Notably, expansion of gene families associated with meristem development is consistent with the presence of below-ground crown buds that enable rapid regeneration after mountain fires. Unexpectedly, we detected tandem duplication and diversification of the strigolactone receptor gene D14, which regulates secondary shoot formation, but not of its ancestral paralog KAI2, which mediates seed germination in response to the smoke-derived compound karrikin. This finding suggests divergent signaling mechanisms underlying fire adaptation across different parasitic plant lineages. By integrating time-series transcriptomic data, we propose a post-fire "defense first, repair later, recovery last" model, in which resources are reallocated from immediate defense to rapid repair and ultimately to long-term recovery, to explain the adaptation of T. ramosoides to fire-prone habitats. Our study provides critical insights into the complex and contrasting genomic dynamics that drive adaptation to multiple co-occurring selection pressures.

Genome, Plant