Plant aquaporin (AQP), one of the ancient protein superfamilies with high diversity, plays a canonical role as water channel transporters to regulate seed germination, stomatal movement, cell elongation, reproduction, and environmental adaptation. Previously, we have demonstrated that two AQPs colocalize within a quantitative trait locus (QTL) linked to the genetic regulation of rose prickles, which function as water reservoirs at their early developmental stages. Here, we systematically characterize the diversity of AQPs in all plant lineages taking the Rosaceae as one example and establish a genetic link between PIP2;1 expression and prickle development. We reveal the ancient origin and remarkable deep conservation in AQP protein structure, the increase of copy number following the diversification of plant lineages and a strong positive selection of the PIP2 and the SIP subfamilies within Rosaceae. Intriguingly, this is contrasted by substantial expression divergence, which is accompanied with regulatory divergence, particularly in cis-regulatory elements associated with hormone responses and developmental regulation. Spatial–temporal expression profiling demonstrates dynamic AQP expression patterns during development of prickle and the underlying cortical tissue in the prickly Rosa gigantea, while also differ substantially in shoots and leaves of the prickly Rosa chinensis and prickle-free Rosa wichuraiana. Silencing the expression of PIP2;1 within the prickle QTL region significantly attenuates the prickle production along rose stems. Our findings not only highlight both evolutionary conservation in AQP protein architecture and lineage-specific regulatory innovation in Rosaceae but also uncover a novel regulatory role of PIP2;1 in epidermal differentiation of the non-model roses, and of likely many other spiny angiosperms.

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