The boron transporter BnaC4.BOR1;1c is critical for inflorescence development and fertility under boron limitation in Brassica napus

Abstract

Boron (B) is an essential micronutrient for plants, but the molecular mechanisms underlying the uptake and distribution of B in allotetraploid rapeseed (Brassica napus) are unclear. Here, we identified a B transporter of rapeseed, BnaC4.BOR1;1c, which is expressed in shoot nodes and involved in distributing B to the reproductive organs. Transgenic Arabidopsis plants containing a BnaC4.BOR1;1c promoter-driven GUS reporter gene showed strong GUS activity in roots, nodal regions of the shoots and immature floral buds. Overexpressing BnaC4.BOR1;1c in Arabidopsis wild type or in bor1-1 mutants promoted wild-type growth and rescued the bor1-1 mutant phenotype. Conversely, knockdown of BnaC4.BOR1;1c in a B-efficient rapeseed line reduced B accumulation in flower organs, eventually resulting in severe sterility and seed yield loss. BnaC4.BOR1;1c RNAi plants exhibited large amounts of disintegrated stigma papilla cells with thickened cell walls accompanied by abnormal proliferation of lignification under low-B conditions, indicating that the sterility may be a result of altered cell wall properties in flower organs. Taken together, our results demonstrate that BnaC4.BOR1;1c is a AtBOR1-homologous B transporter gene expressing in both roots and shoot nodes that is essential for the developing inflorescence tissues, which highlights its diverse functions in allotetraploid rapeseed compared with diploid model plant Arabidopsis.

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

“…Brassica napus cv. Qingyou10 ( Q10 ) and Westar10 ( W10 ) are B‐efficient and B‐inefficient cultivars, respectively, and served to study physiological, molecular and genetic factors influencing B efficiency (Zhao et al ., ; Yang et al ., ; Zhang et al ., ,b, ; Yuan et al ., ; Zhou et al ., ).…”

“…Another study suggested that transcript and protein abundance of BnaC04.BOR1;1c adds to the B deficiency tolerance of cv. Q10 due to the fact that a knockdown mutant suffered from severe shoot and flower B deficiency symptoms when grown in B-deficient growth conditions (Zhang et al, 2017;Chen et al, 2018).…”

“…It is completely unknown which BnaNIPs facilitate the transmembrane diffusion of B and which ones not. BnaC04.BOR1;1c is the only isoform for which B transport activity has been suggested based on the analyses of BnaC04.BOR1;1c overexpressing and silenced plants (Zhang et al, 2017;Chen et al, 2018).…”

Boron and its compounds: current biological research activities

“…Other research milestones included the identification of a boric acid channel, NIP5;1, and a boric acid/borate exporter, BOR1, from Arabidopsis thaliana (Takano et al 2008). There is increasing evidence that the boron transporters are generally important for plant development, for instance in roots and shoot nodes and for the development of inflorescence tissues (Zhang et al 2017).…”

Preferential Distribution of Boron to Developing Tissues Is Mediated by the Intrinsic Protein OsNIP3

“…In Arabidopsis, NIP5;1 and BOR1 are polarly localized at the distal and proximal side of the plasma membrane of the root cells, respectively (Takano et al, 2010), and their cooperative transport is required for efficient and directional uptake of B in the roots especially under a B-limited condition Reid 2014). Homologs of Arabidopsis NIP5;1 and BOR1 have been functionally characterized in other plant species such as rice (Oryza sativa), barley (Hordeum vulgare), rapeseed (Brassica napus), and maize (Zea mays; Nakagawa et al, 2007;Sutton et al, 2007;Chatterjee et al, 2014;Durbak et al, 2014;Hanaoka et al, 2014;Leonard et al, 2014;Zhang et al, 2017). Basically, they have a similar role in B uptake, although the expression patterns differ somewhat within plant species.…”