Nodulin Intrinsic Protein 7;1 Is a Tapetal Boric Acid Channel Involved in Pollen Cell Wall Formation

Abstract

Boron is an essential plant micronutrient that plays a structural role in the rhamnogalacturonan II component of the pectic cell wall. To prevent boron deficiency under limiting conditions, its uptake, distribution, and homeostasis are mediated by boric acid transporters and channel proteins. Among the membrane channels that facilitate boric acid uptake are the type II nodulin intrinsic protein (NIP) subfamily of aquaporin-like proteins. Arabidopsis (Arabidopsis thaliana) possesses three NIP II genes (NIP5;1, NIP6;1, and NIP7;1) that show distinct tissue expression profiles (predominantly expressed in roots, stem nodes, and developing flowers, respectively). Orthologs of each are represented in all dicots. Here, we show that purified and reconstituted NIP7;1 is a boric acid facilitator. By using native promoter-reporter fusions, we show that NIP7;1 is expressed predominantly in anthers of young flowers in a narrow developmental window, floral stages 9 and 10, with protein accumulation solely within tapetum cells, where it is localized to the plasma membrane. Under limiting boric acid conditions, loss-of-function T-DNA mutants (nip7;1-1 and nip7;1-2) show reduced fertility, including shorter siliques and an increase in aborted seeds, compared with the wild type. Under these conditions, nip7;1 mutant pollen grains show morphological defects, increased aggregation, defective exine cell wall formation, reduced germination frequency, and decreased viability. During stages 9 and 10, the tapetum is essential for supplying materials to the pollen microspore cell wall. We propose that NIP7;1 serves as a gated boric acid channel in developing anthers that aids in the uptake of this critical micronutrient by tapetal cells.

Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26‐like Intrinsic Proteins and BOR1 transporters

“…This cooperative system ensures root B uptake, B rootto-shoot translocation and B loading into specific cells, tissues or the apoplast of different model and crop plant species (Takano et al, 2006;Miwa et al, 2007;Reid, 2007;Sutton et al, 2007;Tanaka et al, 2008;Kajikawa et al, 2011;Miwa et al, 2013;Chatterjee et al, 2014Chatterjee et al, , 2017Durbak et al, 2014;Hanaoka et al, 2014;Pallotta et al, 2014;Hua et al, 2016a;Routray et al, 2018;Shao et al, 2018). Additionally, BORs and NIPs have been demonstrated to be decisive factors determining plant B toxicity tolerance (Miwa and Fujiwara, 2010).…”

Boron: More Than an Essential Element for Land Plants?

“…Flowers are singular organs representing the last developmental phases; therefore, it is not surprising that efforts should be made to understand flower development and the roles B plays in this process, which is an exciting yet understudied field of plant biology. It has been demonstrated that NIP7;1, a facilitator of boric acid transport, is predominantly expressed in young flower anthers in a narrow developmental window ( Routray et al, 2018 ). Accordingly, nip7;1 mutants exhibit several defects in reproductive structures ( Routray et al, 2018 ), indicating that proper control of B homoeostasis in both meristem and reproductive organs is critical for the biological success of vascular plants.…”

“…It has been demonstrated that NIP7;1, a facilitator of boric acid transport, is predominantly expressed in young flower anthers in a narrow developmental window ( Routray et al, 2018 ). Accordingly, nip7;1 mutants exhibit several defects in reproductive structures ( Routray et al, 2018 ), indicating that proper control of B homoeostasis in both meristem and reproductive organs is critical for the biological success of vascular plants. Thus, this evidence suggests that obtaining and maintaining an optimal B level in flower-related tissues is often imperative for successful plant reproduction.…”

How Plants Handle Trivalent (+3) Elements

“…Contrastingly, NIP6;1, which is mainly expressed in stems, is impermeable to water and is responsible for distribution of B in the growing shoot tissues [87]. NIP7;1, with strong expression in floral tissues, seems to favor B-transport to the developing tapetal tissue of developing anthers [88].…”