Fungal and plant gene expression in the Tulasnella calospora–Serapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas

Abstract

Summary Orchids are highly dependent on their mycorrhizal fungal partners for nutrient supply, especially during early developmental stages. In addition to organic carbon, nitrogen (N) is probably a major nutrient transferred to the plant because orchid tissues are highly N‐enriched. We know almost nothing about the N form preferentially transferred to the plant or about the key molecular determinants required for N uptake and transfer. We identified, in the genome of the orchid mycorrhizal fungus Tulasnella calospora, two functional ammonium transporters and several amino acid transporters but found no evidence of a nitrate assimilation system, in agreement with the N preference of the free‐living mycelium grown on different N sources. Differential expression in symbiosis of a repertoire of fungal and plant genes involved in the transport and metabolism of N compounds suggested that organic N may be the main form transferred to the orchid host and that ammonium is taken up by the intracellular fungus from the apoplatic symbiotic interface. This is the first study addressing the genetic determinants of N uptake and transport in orchid mycorrhizas, and provides a model for nutrient exchanges at the symbiotic interface, which may guide future experiments.

Nitrogen transport in the orchid mycorrhizal symbiosis – further evidence for a mutualistic association

“…The research presented by Fochi et al . also provides a new perspective on orchid to fungal nutrient transport. Cameron et al .…”

“…Tulasnella calospora is a cosmopolitan orchid mycorrhizal fungus, colonizing many photosynthetic species in Europe, North America, South America, Australia and Asia (reviewed in Dearnaley, ). Fochi et al . cultured T. calospora on a variety of media containing different sources of N. As evidenced by comparisons of mycelial dry weight, the fungus grew best on organic N sources, such as glutamine and glutamic acid and ammonium‐based media, but grew poorly on media containing sodium nitrate. Searches of the T. calospora genomic database identified two functional ammonium transporters but no nitrate uptake and assimilation genes.…”

“…(), utilizing cellular level imaging of stable isotope tracers suggested that 15 NH 4 15 NO 3 passed from mycorrhizal fungus to orchid across intact pelotons. Fochi et al . investigated fungal and plant amino acid transport genes in free‐living mycelium of T. calospora and asymbiotic and symbiotic protocorms of S. vomeracea . These investigations showed that a number of fungal amino acid transporters/permeases (TcAAT1, TcAAT2, TcAAT6) were significantly upregulated in the symbiotic situation.…”

Mycorrhizal fungi affect orchid distribution and population dynamics

“…Additional differences among OMFs have been suggested by recent genome (Zuccaro et al ., ; Kohler et al ., ) and transcriptome (Fochi et al ., , ; M. K. McCormick, unpublished data) studies demonstrating that OMFs differed genetically in their ability to access nutrient and carbon sources. In particular, fungi in the genus Tulasnella and some Serendipita lacked the genes to access nitrate and nitrite, while fungi belonging to Ceratobasidium have multiple genes for accessing nitrate and nitrite.…”

“…Taken together, this evidence suggests that OMF species differ in ability to support orchids among habitats and climatic conditions (McCormick et al ., ; Kohler et al ., ; Fochi et al ., ; Mujica et al ., ). Genotypic and epigenetic differences among strains of OMFs may also affect their ability to support orchids.…”