Triparental plants provide direct evidence for polyspermy induced polyploidy

Abstract

It is considered an inviolable principle that sexually reproducing organisms have no more than two parents and fertilization of an egg by multiple sperm (polyspermy) is lethal in many eukaryotes. In flowering plants polyspermy has remained a hypothetical concept, due to the lack of tools to unambiguously identify and trace this event. We established a high-throughput polyspermy detection assay, which uncovered that supernumerary sperm fusion does occur in planta and can generate viable polyploid offspring. Moreover, polyspermy can give rise to seedlings with one mother and two fathers, challenging the bi-organismal concept of parentage. The polyspermy derived triploids are taller and produce bigger organs than plants resulting from a regular monospermic fertilization. In addition, we demonstrate the hybridization potential of polyspermy by instantly combining three different Arabidopsis accessions in one zygote. Our results provide direct evidence for polyspermy as a route towards polyploidy, which is considered a major plant speciation mechanism.

Reproduction: Plant Parentage à Trois

“…Whether rare natural instances of triparental polyploidy due to break down of the egg cell polyspermy barrier are an important mode of speciation, as Nakel et al propose [8], remains to be shown. Polyploidization is considered a major driver of plant evolution, as up to 70% of flowering plant species are of polyploid origin [14].…”

“…Meanwhile, Rita Groß-Hardt's group set up an independent system they call high-throughput polyspermy detection (HIPOD) to show that polyspermy results in viable polyploids in Arabidopsis at a rate of 0.012% [8]. In their approach, only seedlings inheriting a GAL4 driver and a UAS target from two independent sperm cells can survive herbicide selection.…”

Polyspermy in angiosperms: Its contribution to polyploid formation and speciation

“…In natural and cultivated populations of flowering plants, however, polyspermy has long remained a hypothetical concept because tools to detect naturally occurring polyspermy in higher plants have been lacking (Tekleyohans, Mao, Kägi, Stierhof, & Groß-Hardt, 2017). A recent breakthrough in experimental techniques has confirmed the production of progenies consisting of one mother and two fathers via heteropollination (-fertilization) in Arabidopsis (Nakel et al, 2017).…”

“…In contrast to animals, polyspermic zygotes of angiosperms can undergo nuclear/cell division and embryonic development with subsequent development into triploid plants (Toda, Ohnishi, & Okamoto, ). Furthermore, triparental progenies can be produced via heteropollination derived possible polyspermy in plants (Nakel et al, ). These reports all indicate that the emergence of triploid progenies via polyspermy among diploid populations is a significant factor in polyploidization, speciation and plant evolution.…”

New advances and future directions in plant polyspermy

“…Such technique provides a powerful tool to study developmental profiles of polyspermic zygotes, embryos, and plants (reviewed by Toda et al in this issue). To address naturally occurring polyspermy events, Nakel et al () took advantage of the GAL4/UAS two‐component system adapted from yeast. Their high‐throughput polypaternal breeding design comprises of one plant line containing the GAL4 transcription factor under a ubiquitous promoter and a second plant line containing the GAL4 responsive UAS enhancer driving a YFP ‐tagged herbicide resistance gene.…”