The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes
Sergio M. de Faria, Jens J. Ringelberg, Eduardo Gross, Erik J. M. Koenen, Domingos Cardoso, George K. D. Ametsitsi, John Akomatey, Marta Maluk, Nisha Tak, Hukam S. Gehlot, Kathryn M. Wright, Neung Teaumroong, Pongpan Songwattana, Haroldo C. de Lima, Yves Prin, Charles E. Zartman , Janet I. Sprent, Julie Ardley, Colin E. Hughes and Euan K. James
Nitrogen-fixing symbiosis is globally important in ecosystem functioning and agriculture,
yet the evolutionary history of nodulation remains the focus of considerable debate. Recent
evidence suggesting a single origin of nodulation followed by massive parallel evolutionary
losses raises questions about why a few lineages in the N2-fixing clade retained nodulation
and diversified as stable nodulators, while most did not. Within legumes, nodulation is
restricted to the two most diverse subfamilies, Papilionoideae and Caesalpinioideae, which
show stable retention of nodulation across their core clades.
We characterize two nodule anatomy types across 128 species in 56 of the 152 genera of
the legume subfamily Caesalpinioideae: fixation thread nodules (FTs), where nitrogen-fixing
bacteroids are retained within the apoplast in modified infection threads, and symbiosomes,
where rhizobia are symplastically internalized in the host cell cytoplasm within membrane-bound symbiosomes (SYMs).
Using a robust phylogenomic tree based on 997 genes from 147 Caesalpinioideae genera,
we show that losses of nodulation are more prevalent in lineages with FTs than those with
We propose that evolution of the symbiosome allows for a more intimate and enduring
symbiosis through tighter compartmentalization of their rhizobial microsymbionts, resulting in
greater evolutionary stability of nodulation across this species-rich pantropical legume clade.