Cell‐type‐specific PIN‐FORMED 3‐mediated polar auxin transport regulates cambial activity and tension wood formation in Populus tomentosa

Auxin is a central regulator of tree secondary growth and forms maxima in the vascular cambium, yet how these maxima are established remains elusive. Here, we functionally characterized two redundant PIN-FORMED 3 (PIN3) paralogs from Populus tomentosa to define their roles in secondary growth and gravity-induced tension wood (TW) formation. We employed fluorescent reporter lines, clustered regularly interspaced short palindromic repeats-generated knockout mutants, phloem-specific RNA interference transgenic plants and isotopic auxin transport assays to dissect PIN3 functions during secondary growth of poplar stems. Loss of function of PIN3 paralogs severely compromises cambial proliferation, secondary xylem differentiation and TW development. PIN3 proteins display cell-type-specific polar localization with basal polarity in phloem cells and outer lateral polarity in endodermal cells. Phloem-expressed PIN3 facilitates basipetal auxin transport and is required for cambial auxin response. Upon gravistimulation, endodermal PIN3 repolarizes along the gravity vector, correlating with TW formation. Our findings identify a cell-type-specific, PIN3-mediated auxin transport mechanism that contributes to auxin-driven secondary growth of tree stems.