Lotus japonicus Symbiosis Genes Impact Microbial Interactions between Symbionts and Multikingdom Commensal Communities

Abstract

Studies on symbiosis genes in plants typically focus on binary interactions between roots and soilborne nitrogen-fixing rhizobia or mycorrhizal fungi in laboratory environments. We utilized wild type and symbiosis mutants of a model legume, grown in natural soil, in which bacterial, fungal, or both symbioses are impaired to examine potential interactions between the symbionts and commensal microorganisms of the root microbiota when grown in natural soil. This revealed microbial interkingdom interactions between the root symbionts and fungal as well as bacterial commensal communities. Nevertheless, the bacterial root microbiota remains largely robust when fungal symbiosis is impaired. Our work implies a broad role for host symbiosis genes in structuring the root microbiota of legumes.

The symbiotic capacity of rhizobium shapes root-associated microbiomes

“…These families included Burkholderiaceae, which contained some species able to form symbiosis with a certain legumes from the Papilionoideae subfamily [83,84] and also some species dominate soybean nodule [85] or known as a plant growth-promoting strain in non-legume plants [86]. Our results are consistent with other studies that found also a depletion of Burkholderiales in the roots of Lotus symbiosis pathway gene mutants [40,41]. Therefore, we suggest that the effective symbiosis promotes the enrichment of bene cial microbes.…”

“…Interestingly, disrupting symbiosis between B. diazoe ciens and soybean signi cantly reduced bacterial diversity in the rhizosphere and rhizoplane. This result is in line with a recent study on plant SYM mutants documenting a reduction of fungal diversity [41]. Together, these studies suggest that functional symbiosis favors a more diverse root microbiota.…”

“…Rhizobial nodulation genes and plant symbiotic signaling genes, including NF receptor genes and downstream common symbiotic signaling pathway (SYM) genes, which are shared with arbuscular mycorrhizal (AM) symbiosis, are necessary to establish the symbiotic relationship and nodule development [29,30,39]. Previous studies have shown that genetic variation in plant genes encoding the common SYM receptor of in Lotus japonicas [40,41], Glycine max [42,43], Medicago truncatula [44] and the non-leguminous Oryza sativa [45] drive the establishment of distinctive root-associated microbiomes. By contrast, the impact of microbial genetic variation such as in rhizobial nodulation genes on root-associated microbiomes remains unknown.…”

Rhizobium Inoculation Drives the Shifting of Rhizosphere Fungal Community in a Host Genotype Dependent Manner

“…This indicated the genetic traits that control rhizobium symbiosis might be also involved in the regulation of fungal community or rhizosphere fungi (Genre and Russo, 2016). Consistent with our results, a recent paper showed that the key genes in the symbiotic signaling pathway significantly influenced the enrichment of some fungi in both rhizosphere and within the roots (Thiergart et al, 2019).…”

Neighboring plants divergently modulate effects of loss-of-function in maize mycorrhizal phosphate uptake on host physiology and root fungal microbiota

“…However, how maize mycorrhizal microbial community homeostasis is affected by functional AM symbiosis traits is elusive. Recent studies performed with mycorrhizal Lotus japonicus mutants disrupted in the common symbiosis signaling pathway (CSSP) or downstream processes showed that an almost complete depletion of Glomeromycotina taxa and impaired arbuscule formation in roots were accompanied by an enrichment of few Ascomycota fungi and shifts in bacterial communities under greenhouse conditions [42,43]. On the other hand, knocking out CSSP genes didn´t affect the life cycle of the growth-promoting basidiomycete fungus Piriformospora indica (also known as Serendipita indica) in L. japonicus nor did silencing of CCaMK affect bacterial or fungal communities in roots of field-grown Nicotiana attenuata [44,45].…”