Thioredoxins (Trxs) are small ubiquitous regulatory disulfide proteins. Plants have an unusually complex complement of Trxs composed of six well-defined types (Trxs f, m, x, y, h, and o) that reside in different cell compartments and function in an array of processes. The extraplastidic h type consists of multiple members that in general have resisted isolation of a specific phenotype. In analyzing mutant lines in Arabidopsis thaliana, we identified a phenotype of dwarf plants with short roots and small yellowish leaves for AtTrx h9 (henceforth, Trx h9), a member of the Arabidopsis Trx h family. Trx h9 was found to be associated with the plasma membrane and to move from cell to cell. Controls conducted in conjunction with the localization of Trx h9 uncovered another h-type Trx in mitochondria (Trx h2) and a Trx in plastids earlier described as a cytosolic form in tomato. Analysis of Trx h9 revealed a 17-amino acid N-terminal extension in which the second Gly (Gly(2)) and fourth cysteine (Cys(4)) were highly conserved. Mutagenesis experiments demonstrated that Gly(2) was required for membrane binding, possibly via myristoylation. Both Gly(2) and Cys(4) were needed for movement, the latter seemingly for protein structure and palmitoylation. A three-dimensional model was consistent with these predictions as well as with earlier evidence showing that a poplar ortholog is reduced by a glutaredoxin rather than NADP-thioredoxin reductase. In demonstrating the membrane location and intercellular mobility of Trx h9, the present results extend the known boundaries of Trx and suggest a role in cell-to-cell communication.