Sorghum DW1 positively regulates brassinosteroid signaling by inhibiting the nuclear localization of BRASSINOSTEROID INSENSITIVE 2

Abstract

Semi-dwarf traits have been widely introgressed into cereal crops to improve lodging resistance. In sorghum (Sorghum bicolor L. Moench), four major unlinked dwarfing genes, Dw1-Dw4, have been introduced to reduce plant height, and among them, Dw3 and Dw1 have been cloned. Dw3 encodes a gene involved in auxin transport, whereas, Dw1 was recently isolated and identified as a gene encoding a protein of unknown function. In this study, we show that DW1 is a novel component of brassinosteroid (BR) signaling. Sorghum possessing the mutated allele of Dw1 (dw1), showed similar phenotypes to rice BR-deficient mutants, such as reduced lamina joint bending, attenuated skotomorphogenesis, and insensitivity against feedback regulation of BR-related genes. Furthermore, DW1 interacted with a negative regulator of BR signaling, BRASSINOSTEROID INSENSITIVE 2 (BIN2), and inhibited its nuclear localization, indicating that DW1 positively regulates BR signaling by inhibiting the function of BIN2. In contrast to rice and wheat breeding which used gibberellin (GA) deficiency to reduce plant height, sorghum breeding modified auxin and BR signaling. This difference may result from GA deficiency in rice and wheat does not cause deleterious side effects on plant morphology, whereas in sorghum it leads to abnormal culm bending.In crop breeding, breeders have significantly changed plant stature during the selection of improved grain crops. One famous example is the introduction of a semi-dwarf trait into rice and wheat in the 1960s. Compared to normal plants, semi-dwarf plants have lower center of gravity, which increases lodging resistance and thus enables plant to sustain high grain yield. This phenomenon was later referred as the 'green revolution' . The mechanism of semi-dwarfism that contributed to the 'green revolution' was the introduction of mutated alleles of gibberellin (GA) 20-oxidase (semidwarf 1; sd1) in rice 1, 2 and DELLA (Rht) in wheat 3 , encoding a GA biosynthesis enzyme and a dominant repressor of GA signal transduction, respectively. Furthermore, it has also been reported that the semi-dwarfism of barley, caused by the introgression of semi-dwarf 1 (sdw1/denso) into cultivars grown in Europe, probably depends on a defect in an ortholog of rice SD1 4-6 . Such wide usage of GA-related mutations to produce semi-dwarf plants has been possible due to a unique feature of GA. That is, GA deficiency specifically causes a decrease in plant height without deleterious side effects on other morphologies or physiologies, whereas dwarfism caused by other mechanisms often induces undesired phenotypes, such as abnormal leaf structure, abnormal internode elongation, and stunted seeds [7][8][9][10] . Therefore, it is rare that mutations involved in mechanisms other than GA deficiency were used to improve lodging resistance in crop breeding. One rare exception is a semi-dwarf barley mutant containing semi-brachytic 1 (uzu), a weak allele of the brassinosteroid (BR) receptor, which is grown in a limited region of East Asia, including areas...

Sorghum stem aerenchyma formation is regulated by SbNAC_D during internode development

“…Stem internode elongation is repressed during the juvenile phase but increases during the vegetative phase (Kebrom et al, 2017) or following floral initiation (Quinby, 1974). Several genes that regulate sorghum stem growth have been identified including an ABCB1 auxin transporter encoded by Dw3 (Multani et al, 2003), a plasma membrane protein encoded by Dw1 (Hilley et al, 2016;Yamaguchi et al, 2016) that is involved in brassinosteroid signaling and cell proliferation (Hirano et al, 2017), and an AGC kinase encoded by Dw2 (Hilley et al, 2017).…”

The genetic architecture of biomechanical traits in sorghum

“…This led to the use of semidwarf varieties for increased harvest indices and suitability of mechanical harvesting in other cereal crops such as oats ( Avena sativa L.) (Milach, Rines, & Phillips, 2002), barley ( Hordeum vulgare L.) (Xu et al., 2017), and sorghum [ Sorghum bicolor (L.) Moench] (Quinby, 1974; Quinby & Karper, 1954). Unlike in the C 3 grain crops (rice and wheat) where breeders selected for recessive alleles in GA biosynthesis and signaling of GA (Hedden, 2003; Multani et al., 2003), grain sorghum breeders strongly selected for short stature by indirectly selecting for the recessive alleles of Dw1 – 3 (Quinby & Karper, 1954), genes that affect stem growth regulated by brassinosteroid signaling ( Dw1 ) (Hirano et al., 2017), auxin transport ( Dw3 ) (Multani et al., 2003), and AGC kinase ( Dw2 ) (Hilley et al., 2017).…”

ZmCLA4 regulates leaf angle through multiple plant hormone-mediated signal pathways in maize

“…BRs are a group of steroid hormones with a paracrine mode of action that determines important traits, such as plant architecture and have been extensively reported as key regulators of leaf angle in cereals. This conclusion is derived from the numerous BR biosynthesis or signaling mutants investigated in rice, maize, and sorghum with consistently reduced leaf angles (Yamamuro et al , 2000; Morinaka et al , 2006; Sakamoto et al , 2006; Wang et al , 2008; Divi and Krishna, 2009; Makarevitch et al , 2012; Tong et al , 2014; Sun et al , 2015; Best et al , 2016; Feng et al , 2016; Hirano et al , 2017). The study of the BR signaling pathway in Arabidopsis and rice is clear; that is, BR is sensed by BRI1 and its two homologous proteins BRL1 and BRL3.…”