The Boron Efflux Transporter ROTTEN EAR Is Required for Maize Inflorescence Development and Fertility    

Abstract

Although boron has a relatively low natural abundance, it is an essential plant micronutrient. Boron deficiencies cause major crop losses in several areas of the world, affecting reproduction and yield in diverse plant species. Despite the importance of boron in crop productivity, surprisingly little is known about its effects on developing reproductive organs. We isolated a maize (Zea mays) mutant, called rotten ear (rte), that shows distinct defects in vegetative and reproductive development, eventually causing widespread sterility in its inflorescences, the tassel and the ear. Positional cloning revealed that rte encodes a membrane-localized boron efflux transporter, co-orthologous to the Arabidopsis thaliana BOR1 protein.Depending on the availability of boron in the soil, rte plants show a wide range of phenotypic defects that can be fully rescued by supplementing the soil with exogenous boric acid, indicating that rte is crucial for boron transport into aerial tissues. rte is expressed in cells surrounding the xylem in both vegetative and reproductive tissues and is required for meristem activity and organ development. We show that low boron supply to the inflorescences results in widespread defects in cell and cell wall integrity, highlighting the structural importance of boron in the formation of fully fertile reproductive organs.

Transport of Boron by thetassel-less1Aquaporin Is Critical for Vegetative and Reproductive Development in Maize

“…To dissect the effects of impaired B influx and efflux in maize, double mutants were generated between tls1 and rotten ear (rte), the putative B efflux transporter in maize (Chatterjee et al, 2014). rte has developmental phenotypes similar though less severe than tls1, with the exception that rte is sterile.…”

“…As HI soils, particularly in Molokai, have high B levels (Hue et al, 1988;Chatterjee et al, 2014) and MO soils may be B deficient (Shorrocks, 1997), we tested the hypothesis that tls1 mutants had a more severe phenotype in MO than HI due to low soil B content in MO. We determined amounts of B at several field sites in MO that were all found to be B deficient (0.41 ppm 6 0.05 SE, n = 6), as it is recommended to apply B to field maize when soil levels are <0.75 ppm (Heckman, 2009).…”

Boron Transport in Maize

“…The tassel-less1 (tls1) mutant (Durbak et al, 2014) shows reduced tassel development and defects in inflorescence meristems, as well as vegetative defects when grown in low-B soil (see figure). Similarly, the maize rotten ear (rte) mutant (Chatterjee et al, 2014) shows vegetative and reproductive defects, including sterility. In Arabidopsis thaliana, B moves into the root via diffusion or active transport by NOD26-LIKE MAJOR INTRINSIC PROTEIN5;1 (NIP5;1).…”

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

“…Basically, they have a similar role in B uptake, although the expression patterns differ somewhat within plant species. Recently, two maize mutants (tls1 and rte) defective in vegetative and inflorescence development were also found to be caused by loss of function of genes homologous to NIP5;1 and BOR1, respectively (Chatterjee et al, 2014;Durbak et al, 2014), highlighting the importance of B in plant growth and development. In addition, some PIPs (plasma membrane intrinsic proteins) such as OsPIP2;4 and OsPIP2;7 in rice (Kumar et al, 2014), ZmPIP1 in maize (Dordas and Brown, 2001), and HvPIP1;3 and HvPIP1;4 in barley (Fitzpatrick and Reid, 2009), have been implicated in B uptake.…”

“…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.…”