SUMMARY: The section Alatae of genus Lemna of the monocotyledonous aquatic duckweed family (Lemnaceae) consists of rather diverse accessions with unknown phylogeny and unclear taxonomic assignment. In contrast to other duckweeds, some Alatae accessions, in addition to mainly vegetative propagation, produce readily flowers and viable seeds. We analyzed the genomic diversity and phylogenetic relationship of 52 Alatae accessions. For this purpose, we applied multiple molecular and cytogenetic approaches, including plastid and nuclear sequence polymorphisms, chromosome counting, genome size determination, and genomic in situ hybridization in combination with geographic distribution. We uncovered ploidy variation, recurrent hybridization, and backcrosses between species and their hybrids. The latter successfully spread over three continents. The results elucidate the evolution of Alatae accessions and explain the difficult taxonomic assignment of distinct accessions. Our study might be an example for analogous studies to resolve the hitherto unclear relationships among accessions of the duckweed genera Wolffiella and Wolffia .

Summary: The cosmopolitan, mainly vegetatively propagating, organ‐reduced monocotyledonous aquatic duckweeds are the smallest and fastest growing angiosperms, distributed world‐wide and flower rarely in nature. Recently, we reported intra‐ and interspecific hybrids and ploidy variants in the genus Lemna . Thus, contrary to the expectation, sexual propagation may occasionally occur within and between Lemna species. Our main goal was to uncover whether the ecologically successful hybrids are evolutionary dead ends or initiate further speciation and novel sexual recombination. We investigated flower development, pollen viability, seed set, and seed germination in hybrids and their parental species and characterized genome size and genetic markers in the progenies. Intraspecific crosses yielded fertile progeny, but all diploid and triploid interspecific hybrids were male sterile. Only an established allotetraploid hybrid reproduced sexually, while colchicine‐induced allotetraploids from allodiploids did not regain sexual competence so far. We concluded that only established allotetraploid hybrids represent an evolutionary breakthrough in duckweeds. Our results regarding sexual traits within the duckweed genus Lemna and the sexual competence of diverse hybrids pave the way for further investigation in this understudied field, provide fundamental data regarding the evolutionary potential of duckweed hybrids and are important for future breeding efforts on this emerging crop.

The aquatic plant family Lemnaceae, commonly called duckweed or water lentil, has attracted increasing interest in the scientific literature over the past two decades. It holds extraordinary potential as a new crop due to its multiple applications: as an alternative protein source for feed and food production, as a starch producer for renewable biofuel, and for its capacity to provide valuable ecosystem services. Its high biomass productivity, ability to thrive under a wide range of environmental conditions, lack of requirement for arable land, and aptitude for nutrient recycling from wastewater align with the criteria for future sustainable crops. The Lemnaceae is a small plant family comprising a still uncertain number of species and hybrids with largely unexplored genetic diversity, owing to its taxonomic complexity. We focus on critical aspects that must be addressed to establish duckweed as a viable crop: the availability and accessibility of genomic resources to understand the genetic basis of key agronomic traits; the development of protocols for flower induction and crossing; and the establishment of effective methods for genetic transformation and plant regeneration, all aimed at enabling selection and breeding strategies. We highlight the importance of duckweed germplasm collections, including accessions from a wide geographic and ecological range, as essential resources for addressing duckweed diversity and supporting both fundamental research and agronomic applications.