Characterization of SIPs-type aquaporins and their roles in response to environmental cues in rice (Oryza sativa L.)

Abstract

Background Aquaporins (AQPs) facilitate water diffusion across biological membranes and are involved in all phases of growth and development. Small and basic intrinsic proteins (SIPs) belong to the fourth subfamily of the plant AQPs. Although SIPs are widely present in higher plants, reports on SIPs are limited. Rice is one of the major food crops in the world, and water use is an important factor affecting rice growth and development; therefore, this study aimed to provide information relevant to the function and environmental response of the rice SIP gene family. Results The rice (Oryza sativa L. japonica) genome encodes two SIP-like genes, OsSIP1 and OsSIP2, whose products are predominantly located in the endoplasmic reticulum (ER) membrane. Heterologous expression in a yeast aquaglyceroporin-mutant fps1Δ showed that both OsSIP1 and OsSIP2 made the cell more sensitive to KCl, sorbitol and H2O2, indicating facilitated permeation of water and hydrogen peroxide. In addition, the yeast cells expressing OsSIP2 were unable to efflux the toxic methylamine taken up by the endogenous MEP permeases, but OsSIP1 showed subtle permeability to methylamine, suggesting that OsSIP1 may have a wider conducting pore than OsSIP2. Expression profiling in different rice tissues or organs revealed that OsSIP1 was expressed in all tissues tested, whereas OsSIP2 was preferentially expressed in anthers and weakly expressed in other tissues. Consistent with this, histochemical staining of tissues expressing the promoter-β-glucuronidase fusion genes revealed their tissue-specific expression profile. In rice seedlings, both OsSIPs were more or less up-regulated under different stress conditions, including osmotic shock, high salinity, unfavorable temperature, redox challenge and pathogen attack, as well as by hormonal treatments such as GA, ABA, MeJA, SA. However, a reduced expression of both OsSIPs was observed under dehydration treatment. Conclusions OsSIP1 and OsSIP2 form the two-member Small Intrinsic Proteins subfamily of aquaporins in rice, they conduct water and H2O2. Moreover, OsSIP1 has a weak ability to conduct methylamine while OsSIP2 does not. Both proteins are mainly localized to the ER, although transient localization to the plasma membrane is not excluded. OsSIP1 is widely expressed in most tissues and during developmental stages, while OsSIP2 expressed preferentially in the anther. Both genes are up-regulated under a variety of stress conditions and by different hormone treatments, except that dehydration moderately reduces their expression. Our results pave the way for further deciphering the unique function of SIP-like aquaporins in substrate transport, growth and development, and environmental response in rice.