PcXTH22 as a core regulator enhancing aluminum toxicity tolerance in Populus cathayana

Aluminum (Al) toxicity in acidic soils restricts plant growth. Xyloglucan endotransglucosylase/hydrolases (XTHs) modulate Al responses, but their mechanisms in poplar remain unknown. Here, we characterized PcXTH22-mediated Al tolerance in Populus cathayana. The PcXTH22OE lines showed negligible injury, whereas the pcxth22 mutants suffered severe damage, confirming the role of PcXTH22 as a positive Al regulator. The pcxth22 lines showed increased xyloglucan endotransglucosylase/hydrolase (XET/XTH) activities and xyloglucan content under Al toxicity. This offered more Al³ ⁺ binding sites and resulted in higher Al accumulation. In contrast, PcXTH22OE lines maintained homeostasis and accumulated less Al. Transcriptomics revealed PcXTH22OE lines upregulated pectin and glucan catabolism genes and downregulated heavy metal-associated isoprenylated plant protein (HIPPs) genes, reducing Al binding and transport. PcXTH22OE lines also showed higher expression of carbohydrate metabolism and brassinosteroid (BR) biosynthesis/signaling genes, while mutants showed opposite trends. Furthermore, we identified PcDOF8 and PcNAC6, triggered by acidic conditions and Al³ ⁺, to transcriptionally activate PcXTH22. Collectively, PcXTH22, induced by PcDOF8 and PcNAC6, limits Al accumulation and enhances Al tolerance by modulating the cell wall, carbohydrate metabolism, and BR responses. Our findings offer insights into breeding plants tolerant to acidic soils and Al toxicity.