Physiological and transcriptomic regulation of Populus simonii fine roots exposed to a heterogeneous phosphorus environment in soil

Soil phosphorus (P) is usually limited and heterogeneously distributed. However, the physiological and transcriptional mechanisms of the woody plant fine roots to heterogeneous P are still unclear. In this study, a split-root system was used to simulate a heterogeneous P environment; that is, half of the fine roots of Populus simonii were grown under normal Pi conditions (2 mM, Hetero-NP), and the other half were grown under low Pi conditions (0.2 mM, Hetero-LP). Subsequently, the physiological and transcriptomic responses of the fine roots were determined under Hetero-NP and Hetero-LP conditions. The concentrations of ATP, malic acid and citric acid in the Hetero-LP region were lower than those in the Hetero-NP region, but the activity of APs was higher. P. simonii fine roots in the Hetero-NP or Hetero-LP region had larger fine root surfaces and SRL, as well as higher malic acid, citric acid, JA and SA concentrations, than those in the homogeneous Pi supply (Homo-NP or Homo-LP). In addition, the soluble protein and total free amino acid concentrations, as well as the AP, PEPC and MDH activities of P. simonii fine roots in Hetero-NP or Hetero-LP were higher than those in Homo-NP but lower than those in Homo-LP. GO, KEGG and MapMan analyses of the differentially expressed genes revealed that the genes in the “metabolic process” term and “plant hormone signal transduction” pathway, as well as in the “RNA”, “protein” and “signalling” categories, play key roles in the response of P. simonii fine roots to heterogeneous Pi. Our results indicated that the response of P. simonii fine roots to Hetero-NP or Hetero-LP differ due to local and systematic regulation. Phytohormones and the MAPK signaling system are involved in the local and systematic response of P. simonii fine roots to heterogeneous Pi supplies by promoting fine root elongation and regulating metabolic processes. Taken together, the findings of this study provide new insights into the response of woody plant fine roots to heterogeneous Pi. •Uncover the mechanisms underlying P. simonii fine roots adaption to heterogeneous P.•Adaptive mechanisms depend on fine root elongation and metabolic changes.•MAPK involves in the regulation of P. simonii fine roots adaptation to heterogeneous P.•Reveal the difference of P. simonii fine roots response to Hetero-NP and Hetero-LP.