The Combined Action of Duplicated Boron Transporters Is Required for Maize Growth in Boron-Deficient Conditions

Abstract

The micronutrient boron is essential in maintaining the structure of plant cell walls and is critical for high yields in crop species. Boron can move into plants by diffusion or by active and facilitated transport mechanisms. We recently showed that mutations in the maize boron efflux transporter ROTTEN EAR (RTE) cause severe developmental defects and sterility. is part of a small gene family containing five additional members (-) that show tissue-specific expression. The close paralogous gene encodes a protein with 95% amino acid identity with RTE and is similarly expressed in shoot and root cells surrounding the vasculature. Despite sharing a similar function with, mutations in the gene do not cause growth defects in the shoot, even in boron-deficient conditions. However, mutants strongly enhance the phenotype in soils with low boron content, producing shorter plants that fail to form all reproductive structures. The joint action of RTE and RTE2 is also required in root development. These defects can be fully complemented by supplying boric acid, suggesting that diffusion or additional transport mechanisms overcome active boron transport deficiencies in the presence of an excess of boron. Overall, these results suggest that and function are essential for maize shoot and root growth in boron-deficient conditions.

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 root‐to‐shoot translocation and B loading into specific cells, tissues or the apoplast of different model and crop plant species (Takano et al ., ; Miwa et al ., ; Reid, ; Sutton et al ., ; Tanaka et al ., ; Kajikawa et al ., ; Miwa et al ., ; Chatterjee et al ., , ; Durbak et al ., ; Hanaoka et al ., ; Pallotta et al ., ; Hua et al ., ; Routray et al ., ; Shao et al ., ). Additionally, BORs and NIPs have been demonstrated to be decisive factors determining plant B toxicity tolerance (Miwa and Fujiwara, ).…”

Increased transpiration is correlated with reduced boron deficiency symptoms in the maize tassel‐less1 mutant

“…Studies regarding the interaction of B with other environmental factors are limited, especially in maize. The recent cloning and characterization of the genes responsible for B uptake/import, namely tls1 (Durbak et al 2014, Leonard et al 2014) and B export, namely rte and rte2 (Chatterjee et al 2014(Chatterjee et al , 2017) enables the study not only of the role(s) of B in plants but also the interaction between B deficiency and other abiotic stresses. Mutants lacking those genes can be rescued by B supplementation in the field as well as in the greenhouse (Chatterjee et al 2014, Durbak et al 2014, Leonard et al 2014.…”

“…The severe vegetative defects of tls1 mutants can be seen in the summer in our field site in Missouri (MO), USA, whereas only the reproductive phenotypes can be seen in our winter nursery in Molokai, Hawaii (HI), USA or in the greenhouse in MO. rte single and rte;rte2 double mutants show similar inflorescence phenotypes as tls1 mutants (Chatterjee et al , ). The drastic inflorescence phenotypes of these B deficient mutants provide an explanation for why yield is reduced under B deficient conditions even in normal maize plants (Lordkaew et al ).…”

“…The drastic inflorescence phenotypes of these B deficient mutants provide an explanation for why yield is reduced under B deficient conditions even in normal maize plants (Lordkaew et al ). All of the phenotypes of tls1 and rte single mutants and rte; rte2 double mutants can be rescued with B supplementation, indicating that the primary defects are due to B deficiency (Chatterjee et al , , Durbak et al , Leonard et al ).…”

“…The underlying B transporter genes BOR1 and NIP5;1 were initially characterized in Arabidopsis thaliana (Arabidopsis) (Noguchi et al 1997, Takano et al 2002, Fujiwara et al 2006 and have recently been cloned in Zea mays (maize). In maize, the co-orthologous gene for the B importer NIP5;1 is called tassel-less1 (tls1) (Durbak et al 2014, Leonard et al 2014, while duplicate genes have been found and characterized for BOR1 called rotten ear (rte) and rte2 (Chatterjee et al 2014(Chatterjee et al , 2017. Through studies of the tls1 mutant, which is inherently B deficient, we discovered that meristems, groups of stem cells that lead to the development of all aboveground organs, are specifically sensitive to B deficiency (Durbak et al 2014).…”