Morphological, genotypic and metabolomic signatures confirm interfamilial hybridization between the ubiquitous kelps Macrocystis (Arthrothamnaceae) and Lessonia (Lessoniaceae)

Murúa, Pedro and Edrada-Ebel, Ru Angelie and Muñoz, Liliana and Soldatou, Sylvia and Legrave, Nathalie and Müller, Dieter G. and Patiño, David J. and van West, Pieter and Küpper, Frithjof C. and Westermeier, Renato and Ebel, Rainer and Peters, Akira F. (2020) Morphological, genotypic and metabolomic signatures confirm interfamilial hybridization between the ubiquitous kelps Macrocystis (Arthrothamnaceae) and Lessonia (Lessoniaceae). Scientific Reports, 10 (1). 8279. ISSN 2045-2322 (https://doi.org/10.1038/s41598-020-65137-3)

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Abstract

Macrocystis pyrifera and Lessonia spicata are economically and ecologically relevant brown seaweeds that recently have been classified as members of two separated families within Laminariales (kelps). Here we describe for the first time the Macrocystis pyrifera x Lessonia spicata hybridization in the wild (Chiloe Island, Southeastern Pacific), where populations of the two parents exist sympatrically. Externally, this hybrid exhibited typical features of its parents M. pyrifera (cylindrical and flexible distal stipes, serrate frond margins and presence of sporophylls) and L. spicata (rigid and flat main stipe and first bifurcation), as well as intermediate features between them (thick unfused haptera in the holdfast). Histological sections revealed the prevalence of mucilage ducts within stipes and fronds (absent in Lessonia) and fully developed unilocular sporangia in the sporophylls. Molecular analyses confirmed the presence of the two parental genotypes for ITS1 nrDNA and the M. pyrifera genotype for two predominantly maternally inherited cytoplasmic markers (COI and rbcLS spacer) in the tissue of the hybrid. A metabolome-wide approach revealed that this hybrid is more chemically reminiscent to M. pyrifera. Nevertheless, several hits were identified as Lessonia exclusive or more remarkably, not present in any of the parent. Meiospores developed into apparently fertile gametophytes, which gave rise to F1 sporophytes that reached several millimeters before suddenly dying. In-vitro reciprocal crossing of Mar Brava gametophytes from both species revealed that although it is rare, interfamilial hybridization between the two species is possible but mostly overcome by pseudogamy of female gametophytes.