KEY MESSAGE:The ER membrane localized aquaporin SIP2;1 is involved in adaptation to ER stresses during pollen tube elongation. Aquaporins play multifaceted roles through selective transport of water and small neutral substrates. Here, we focused on the physiological roles of Arabidopsis thaliana aquaporins, namely SIP1;1, SIP1;2 and SIP2;1, which are localized to the endoplasmic reticulum (ER). While their loss-of-function mutants displayed normal vegetative growth. We identified defects in pollen of sip2;1. Whereas the germination rate of sip2;1 pollen was ~ 60% that of the wild type (WT), in vitro germinated sip2;1 pollen tube length was reduced up to 82% compared to the WT. Importantly, most pollen tubes on pistils from sip2;1 stopped elongation in the mid-region of pistils, and the bottom region of sip2;1 siliques lacked seeds. Consistently, silique of sip2;1 were short, whereby the average seed number per silique was nearly the half of the WT. The above phenotypes recovered in SIP2;1 complementation lines. We detected mRNA of SIP2;1 and protein in pollen, and further revealed that the GFP-linked SIP2;1 localization in the ER of growing pollen tubes. The basal mRNA level of BINDING PROTEIN 3 (BiP3), a key gene induced by ER stress, in pollen was markedly higher than that in roots, suggesting that the pollen underwent ER stress under normal growth conditions. BiP3 mRNA was dramatically increased in sip2;1 pollen. Altogether, our findings suggest that the aquaporin SIP2;1 is probably involved in the alleviation of ER stress and that the lack of SIP2;1 reduces both pollen germination and pollen tube elongation.