Mechanisms underlying the heartwood color difference between Catalpa bungei and Catalpa lutea and their correlation with wood properties.

Catalpa bungei C. A. Mey is a precious timber species endemic to China, and its congeneric species Catalpa lutea J.H.Wang, W.J.Ma & Z.Y.Li possesses higher economic value due to its distinctive golden-yellow heartwood. To elucidate the metabolic and molecular mechanisms underlying the heartwood color difference between C. lutea and C. bungei, as well as the potential associations between heartwood color and wood properties, we conducted metabolomic and transcriptomic analyses on the sapwood, transition zone and heartwood of 21-year-old C. bungei and C. lutea trees, and systematically evaluated their wood anatomical structure, physical and mechanical properties, and decay resistance. The results showed that compared with C. bungei, 17 chromogenic metabolites (10 quinones, 7 flavonoids) were significantly accumulated in the heartwood of C. lutea, among which α-lapachone derivatives (especially 9-hydroxy-α-lapachone and 4,9-dihydroxy-α-lapachone) accounted for 69.99% of the total chromogenic substances, representing the major color-contributing compounds in C. lutea heartwood. Through Gene Ontology enrichment analysis and expression profiling, five CbuCYP450 genes with hydroxylation functions, namely CbuCYP86A1 (evm.TU.group330.7), CbuCYP82A3A (evm.TU.group3.584), CbuCYP82A3B (evm.TU.group3.585), CbuCYPH3 (evm.TU.group11.1088) and CbuCYP71D95 (evm.TU.group11.1150) were identified as highly expressed in the transition zone of C. lutea, potentially involved in the hydroxylation steps of α-lapachone-derivative biosynthesis. Wood-property measurements revealed that, compared with C. bungei, C. lutea possessed significantly higher double wall thickness and wall-to-lumen ratio in fiber cells, as well as significantly superior wood density, hardness, compressive and tensile strengths, and natural decay resistance. The biosynthesis of the identified chromogenic metabolites, particularly α-lapachone and its derivatives, may be associated with the high expression of CbuCYP71D95 and other CbuCYP450 genes. Furthermore, the anatomical structure characterized by thick-walled and narrow-lumened cells, together with the abundant secondary metabolites, jointly endow C. lutea with excellent mechanical properties and decay resistance. This study provides a theoretical foundation for the color-targeted breeding of C. bungei and C. lutea and for the high-value genetic improvement of precious timber species.