The dark septate endophyte Phialocephala sphaeroides confers growth fitness benefits and mitigates pathogenic effects of Heterobasidion on Norway spruce

Abstract

Forest trees frequently interact with a diverse range of microorganisms including dark septate root endophytes (DSE) and fungal pathogens. Plant defense response to either individual pathogen or endophyte has been widely studied, but very little is known on the effect of coinfection on host defenses. To study the impact of coinfection or tripartite interaction on plant growth and host defenses, Norway spruce (Picea abies) seedlings were inoculated with a DSE Phialocephala sphaeroides or with a root pathogen Heterobasidion parviporum, or coinfected with both fungi. The results showed that the root endophyte promoted the root growth of spruce seedlings. Control seedlings without any inoculum were subjected to sequencing and used as a baseline for identification of differentially expressed genes. RNA-Seq analysis of seedlings inoculated with P. sphaeroides, infected with H. parviporum or coinfected with both fungi resulted in a total of 5,269 differentially expressed genes (DEGs). The majority of DEGs were found in P. sphaeroides-inoculated seedlings. Lignin biosynthesis pathways were generally activated during fungal infections. The pattern was distinct with endophyte inoculation. The majority of the genes in the flavonoid biosynthesis pathway were generally suppressed during fungal infections. A specific transcriptional response to P. sphaeroides inoculation was the increased transcripts of genes involved in jasmonic acid biosynthesis, MAPK signaling pathway, plant hormone signal transduction, and calcium-mediated signaling. This may have potentially contributed to promoting the root growth of seedlings. Although the coinfection suppressed the induction of numerous genes, no negative effect on the growth of the spruce seedlings occurred. We conclude that the subsequent H. parviporum infection triggered reprogramming of host metabolism. Conversely, the endophyte (P. sphaeroides), on the other hand, counteracted the negative effects of H. parviporum on the growth of the spruce seedlings.

The dark septate endophyte Phialocephala sphaeroides suppresses conifer pathogen transcripts and promotes root growth of Norway spruce

“…2022 ) and fungi were sequenced. The results supplement the earlier published findings on the host transcriptome ( Wen et al. 2022 ).…”

“…The total RNAs include the RNAs from Norway spruce, P. sphaeroides and/or H. parviporum . The co-cultivation, RNA isolation and RNAseq were conducted as previously described ( Wen et al. 2022 ).…”

“…The physiological and metabolic changes of PGP microbes and antagonistic microbes are largely unknown. Wen et al. (2022 ) recently reported that Norway spruce seedlings inoculated with DSE P. sphaeroides exhibited PGP effect in promoting primary root elongation.…”

“…In addition, there was no negative effect on seedlings co-infected with both the endophyte and pathogen Heterobasidion parviporum , compared with those infected with pathogen alone. In addition, multiple host transcriptional responses in Ps-inoculated seedlings could have contributed to the root growth promotion ( Wen et al. 2022 ).…”

“…Norway spruce seedlings inoculated with Ps-alone (PaPs), Hp-alone (PaHp), and co-infected with Ps and Hp (PaPsHp) were selected for total RNA isolation. Thus, transcripts of both spruce ( Wen et al. 2022 ) and fungi were sequenced.…”