TY - JOUR
T1 - Soil organic phosphorus is mainly hydrolyzed via phosphatases from ectomycorrhiza-associated bacteria rather than ectomycorrhizal fungi
AU - Yuan, Jing
AU - Yan, Rui
AU - Zhang, Xueqiong
AU - Su, Kai
AU - Liu, Hui
AU - Wei, Xin
AU - Wang, Ran
AU - Huang, Lanlan
AU - Tang, Nianwu
AU - Wan, Shanping
AU - Liu, Wei
AU - Lambers, Hans
AU - Zheng, Yi
AU - He, Xinhua
AU - Yu, Fuqiang
AU - Wang, Yanliang
N1 - Publisher Copyright:
© The Author(s), under exclusive licence to Springer Nature Switzerland AG 2024.
PY - 2024/11
Y1 - 2024/11
N2 - Background and aims: Mycorrhizal fungi-released phosphatases have long been claimed pivotal to mobilize soil organic phosphorus (P). We hypothesized that ectomycorrhizal (ECM) fungi, compared with their saprotrophic ancestors, evolved adaptive strategies to enhance the release of phosphatases to meet the P demand of ECM fungi and their host plants. Methods: We analyzed genes potentially encoding secreted phosphatases in 103 fungal species, ECM fungi hyphae associated- and ectomycorrhizosphere phosphatase enzyme activities, and gene expression of Lactarius spp. and Laccaria bicolor fungi-secreted phosphatases during ECM formation. We also determined ectomycorrhizosphere abundance of bacterial phosphatase genes, and analyzed Pinus yunnanensis–Lactarius deliciosus ectomycorrhiza-associated P-mobilizing bacteria. Results: We found that during transition from saprotrophy to ECM symbiosis, genes encoding fungal-secreted phosphatases did not manifest adaptive or convergent evolution. Among 10 genes potentially encoding secreted fungal phosphatases in Lactarius spp. and Laccaria bicolor, only two were up-regulated during ECM formation. Furthermore, unlike saprotrophic fungi, pure-cultured ECM fungi hyphae released very few or no phosphatases to the surroundings, while ECMs generally increased the phosphatase activities in the ectomycorrhizosphere under glasshouse conditions. Additionally, ECM-associated bacteria exhibited an increased abundance of P-cycling genes in the ectomycorrhizosphere under both glasshouse and field conditions. A substantial part of culturable bacteria from ECM tips hydrolyzed organic P and promoted fungal P acquisition. Conclusion: We found no evidence for adaptive evolution of secreted phosphatases in ECM fungi; some ECM fungi may not even release phosphatases, and ECM-associated bacteria likely play a pivotal role in ECM-promoted organic P hydrolysis and plant P acquisition.
AB - Background and aims: Mycorrhizal fungi-released phosphatases have long been claimed pivotal to mobilize soil organic phosphorus (P). We hypothesized that ectomycorrhizal (ECM) fungi, compared with their saprotrophic ancestors, evolved adaptive strategies to enhance the release of phosphatases to meet the P demand of ECM fungi and their host plants. Methods: We analyzed genes potentially encoding secreted phosphatases in 103 fungal species, ECM fungi hyphae associated- and ectomycorrhizosphere phosphatase enzyme activities, and gene expression of Lactarius spp. and Laccaria bicolor fungi-secreted phosphatases during ECM formation. We also determined ectomycorrhizosphere abundance of bacterial phosphatase genes, and analyzed Pinus yunnanensis–Lactarius deliciosus ectomycorrhiza-associated P-mobilizing bacteria. Results: We found that during transition from saprotrophy to ECM symbiosis, genes encoding fungal-secreted phosphatases did not manifest adaptive or convergent evolution. Among 10 genes potentially encoding secreted fungal phosphatases in Lactarius spp. and Laccaria bicolor, only two were up-regulated during ECM formation. Furthermore, unlike saprotrophic fungi, pure-cultured ECM fungi hyphae released very few or no phosphatases to the surroundings, while ECMs generally increased the phosphatase activities in the ectomycorrhizosphere under glasshouse conditions. Additionally, ECM-associated bacteria exhibited an increased abundance of P-cycling genes in the ectomycorrhizosphere under both glasshouse and field conditions. A substantial part of culturable bacteria from ECM tips hydrolyzed organic P and promoted fungal P acquisition. Conclusion: We found no evidence for adaptive evolution of secreted phosphatases in ECM fungi; some ECM fungi may not even release phosphatases, and ECM-associated bacteria likely play a pivotal role in ECM-promoted organic P hydrolysis and plant P acquisition.
KW - Acid and alkaline phosphatases
KW - Evolution
KW - Gene expression
KW - Phosphorus cycling
KW - Phosphorus-mobilizing bacteria
KW - Saprotrophic fungi
UR - http://www.scopus.com/inward/record.url?scp=85189496848&partnerID=8YFLogxK
U2 - 10.1007/s11104-024-06649-z
DO - 10.1007/s11104-024-06649-z
M3 - Article
AN - SCOPUS:85189496848
SN - 0032-079X
VL - 504
SP - 659
EP - 678
JO - Plant and Soil
JF - Plant and Soil
IS - 1
M1 - 108520
ER -