Assessment of Polygala paniculata (Polygalaceae) characteristics for evolutionary studies of legume\u2013rhizobia symbiosis

Yuji Tokumoto,Tomomi Nakagawa,Mai Fukuhara,Jun Yokoyama,Wataru Iwasaki,Seishiro Aoki,Takashi Soyano,Kazuhiko Saeki,Hironori Fujita,Kayo Hashimoto,Masayoshi Kawaguchi

doi:10.1007/s10265-019-01159-x

Abstract

Root nodule (RN) symbiosis is a mutualistic interaction observed between nitrogen-fixing soil bacteria and nodulating plants, which are scattered in only four orders of angiosperms called nitrogen-fixing clade. Most of legumes engage in RN symbiosis with rhizobia. Molecular genetic analyses with legumes and non-leguminous nodulating plants revealed that RN symbiosis utilizes early signalling components that are required for symbiosis with arbuscular mycorrhizal (AM) fungi. However detailed evolutionary processes are still largely unknown. Comparative analyses with non-nodulating species phylogenetically related to legumes could be better strategies to study the evolution of RN symbiosis in legumes. Polygala paniculata is a non-leguminous species that belongs to a family different from legumes but that is classified into the same order, Fabales. It has appropriate characteristics for cultivation in laboratories: small body size, high fertility and short lifecycles. Therefore, we further assessed whether this species is suitable as a model species for comparative studies with legumes. We first validated that the plant we obtained in Palau was truly P. paniculata by molecular phylogenetic analysis using rbcL sequences. The estimated genome size of this species was less than those of two model legumes, Lotus japonicus and Medicago truncatula. We determined conditions for cultivation in vitro and for hairy root formation from P. paniculata seedlings. It would facilitate to investigate gene functions in this species. The ability of P. paniculata to interact with AM fungi was confirmed by inoculation with Rhizophagus irregularis, suggesting the presence of early signalling factors that might be involved in RN symbiosis. Unexpectedly, branching of root hairs was observed when inoculated with Mesorhizobium loti broad host range strain NZP2037, indicating that P. paniculata has the biological potential to respond to rhizobia. We propose that P. paniculata is used as a model plant for the evolutionary study of RN symbiosis.

Highlights

IntroductionSymbiotic relationships between plants and soil microbes (fungi and bacteria) are a fundamental topic in biology
Symbiotic relationships between plants and soil microbes are a fundamental topic in biology
We found that the estimated genome size of P. paniculata was similar to that of L. japonicus and M. truncatula

Summary

Introduction

Symbiotic relationships between plants and soil microbes (fungi and bacteria) are a fundamental topic in biology. Symbioses between plants and mycorrhizal fungi are common. Extended author information available on the last page of the article among plant taxa; about 70% of flowering plant families form symbiotic relationships with arbuscular mycorrhizal (AM) fungi (Bonfante and Genre 2010; Brundrett 2009; Zhu et al 2006). It has been predicted that genetic predisposition to RN symbiosis was acquired once in a common ancestor of these orders (Doyle 2011; Soltis et al 1999; Werner et al 2014). Phylogenomic analyses conducted in recent studies have shown that RN symbiosis was lost several times independently in ancestral

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