Aging seeds of weedy broomrapes and witchweeds lose sensitivity to strigolactones as DNA demethylates

Abstract

Societal Impact StatementBroomrapes and witchweeds have devastating effects on crops in parts of Europe, Africa, and Asia. The key to their success is the production of copious, long‐lived seeds, which germinate in response to the perception of chemicals released by their hosts' roots. Here, it is proposed that the success of a parasite population will decrease as its seed bank ages due to the gradual decrease in sensitivity to the host signals in correlation with alterations of the seeds' epigenetic landscape, which is the set of non‐hard‐coded genetic information that influences gene function. This research provides important information toward a better understanding of parasite seed bank dynamics, which must be accounted for in future control strategies.Summary Broomrapes (Phelipanche and Orobanche spp.) and witchweeds (Striga and Alectra spp.) are obligate root parasitic weeds responsible for major crop yield losses worldwide. Their success in agricultural landscapes is attributable to their ability to produce thousands of long‐lived minute seeds that coordinate their germination with the presence of nearby hosts by perceiving host‐derived strigolactones. The processes underlying the alleged decade(s)‐long persistence in the field are understudied. Here, we used an accelerated seed aging method coupled with germination bioassays and an enzyme‐linked immunosorbent assay (ELISA), which allowed studying seed aging in Orobanchaceae in a comparative manner. We show that the losses of seed viability and germinability associated with seed aging are accompanied by a decrease in both strigolactone sensitivity and global DNA methylation. Our results also suggest that seeds of broomrapes are longer‐lived than those of witchweeds. Overall, this emphasizes the need for further research into how epigenetic mechanisms contribute to alterations in seed viability in parasitic weeds and how seed aging influences seed responses to their environment.