The genome of the vining fern Lygodium microphyllum highlights genomic and functional differences between life phases of an invasive plant

Abstract

Functional and genomic studies on the differences between gametophyte and sporophyte life phases remain scarce, yet unraveling these dynamics is crucial to understanding the biology of plants and the success of each phase under different environments. Here, we provide a novel reference genome for the highly invasive fern Lygodium microphyllum and compare the transcriptomic and epigenomic landscapes of the gametophyte and sporophyte life phases. We found differential regulation of developmental genes (homeobox and MADS-box clades) and usage of alternative isoforms that may play a role in the genomic determination of the haploid and diploid life stages. We further generated the first base pair-resolution methylome of a fern gametophyte, and determined that methylation patterns are remarkably similar between vegetative tissues despite their morphological and functional differences. By examining the physiological and transcriptomic responses of gametophytes and sporophytes to freezing stress, the most likely abiotic factor preventing further expansion of this invasive species, we show that life phases and tissues use alternative molecular pathways to respond to this stressor, underscoring the need to incorporate both life phases when developing effective mitigation strategies. These new genomic resources fill a gap in our understanding of fundamental plant biology and inform invasive species research. SIGNIFICANCEAll land plants undergo an alternation of generations between haploid gametophyte and diploid sporophyte life phases. How these disparate life phases are generated from a single genome, and the functional implications of these differences for plant success, is largely unknown. Moreover, understanding life-phase-specific differences in rapidly evolving populations, such as invasive species, is critical to developing effective management strategies. We assembled a chromosome-level genome and generated epigenomic and transcriptomic resources from gametophyte and sporophyte phases of the invasive fern Lygodium microphyllum, which is estimated to cost the U.S. more than $2 million annually. We highlight transcriptomic, epigenomic, and physiological variation between life phases and find support for the crucial role of the often overlooked gametophyte in the invasion process.