Gibberellin deficiency pleiotropically induces culm bending in sorghum: an insight into sorghum semi-dwarf breeding

Ordonio, Reynante Lacsamana; Ito, Yusuke; Hatakeyama, Asako; Ohmae-Shinohara, Kozue; Kasuga, Shigemitsu; Tokunaga, Tsuyoshi; Mizuno, Hiroshi; Kitano, Hidemi; Matsuoka, Makoto; Sazuka, Takashi

doi:10.1038/srep05287

Cited by 41 publications

(39 citation statements)

References 59 publications

(89 reference statements)

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“…Furthermore, recent chemical complementation experiments of GA mutants in Sorghum sp. used application of exogenous GA 3 (Ordonio et al, 2014), consistent with the work by Lee et al (1998). Therefore, we hypothesized that the genetic block leading to no bioactive GAs in dwf1-1 could be chemically complemented by application of exogenous GA 3 .…”

Section: Dwf1-1 Phenotype Is Rescued By the Application Of Exogenous supporting

confidence: 59%

Mapping of a Cellulose-Deficient Mutant Named dwarf1-1 in Sorghum bicolor to the Green Revolution Gene gibberellin20-oxidase Reveals a Positive Regulatory Association between Gibberellin and Cellulose Biosynthesis

et al. 2015

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ORCID IDs: 0000-0001-7521-3615 (C.P.); 0000-0002-5473-526X (J.S.).Here, we show a mechanism for expansion regulation through mutations in the green revolution gene gibberellin20 (GA20)-oxidase and show that GAs control biosynthesis of the plants main structural polymer cellulose. Within a 12,000 mutagenized Sorghum bicolor plant population, we identified a single cellulose-deficient and male gametophyte-dysfunctional mutant named dwarf1-1 (dwf1-1). Through the Sorghum propinquum male/dwf1-1 female F2 population, we mapped dwf1-1 to a frameshift in GA20-oxidase. Assessment of GAs in dwf1-1 revealed ablation of GA. GA ablation was antagonistic to the expression of three specific cellulose synthase genes resulting in cellulose deficiency and growth dwarfism, which were complemented by exogenous bioactive gibberellic acid application. Using quantitative polymerase chain reaction, we found that GA was positively regulating the expression of a subset of specific cellulose synthase genes. To cross reference data from our mapped Sorghum sp. allele with another monocotyledonous plant, a series of rice (Oryza sativa) mutants involved in GA biosynthesis and signaling were isolated, and these too displayed cellulose deficit. Taken together, data support a model whereby suppressed expansion in green revolution GA genes involves regulation of cellulose biosynthesis.In all higher plants, development of upright plant growth is advanced by a highly regulated process of cell division, cell fate determination, and cell expansion (Xie et al., 2011). Cell shape and morphogenesis are largely acquired through anisotropic expansion, during which the plant cell wall provides the structural integrity needed to resist internal turgor pressure and simultaneously extend in a controlled and organized manner (Cosgrove and Jarvis, 2012). Cellulose is the main loadbearing component on the plant cell wall, and cellulose is synthesized in a highly organized manner according to the expansion state and growth pattern (Tsekos, 1999). A number of phytohormones are involved in regulating expansion, including auxin (Paque et al., 2014), brassinosteroid (Xie et al., 2011, the rapid alkalinization factor peptide hormone (Haruta et al., 2014), cytokinin (Downes andCrowell, 1998), and GAs (Keyes et al., 1989). A complex and still poorly understood interplay exists among phytohormones to precisely regulate cellular expansion machinery.Sorghum bicolor is one of the most agriculturally important grains produced worldwide (Paterson, 2008). It is largely cultivated in Africa, India, China, and the United States for both grain and biomass. An advantage that Sorghum sp. holds over many other grain crops is drought tolerance, an important trait in low-rainfall conditions and anticipated climate change shifts (Schmidhuber and Tubiello, 2007 (Paterson et al., 2009;Liu and Godwin, 2012). Here, we aimed to isolate a cellulosedeficient mutant from within a chemical mutagenesis population, which we named dwarf1-1 (dwf1-1). From here, we aimed to characterize the geneti...

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Section: Dwf1-1 Phenotype Is Rescued By the Application Of Exogenous supporting

confidence: 59%

Mapping of a Cellulose-Deficient Mutant Named dwarf1-1 in Sorghum bicolor to the Green Revolution Gene gibberellin20-oxidase Reveals a Positive Regulatory Association between Gibberellin and Cellulose Biosynthesis

et al. 2015

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“…Rice and wheat can repress GA signaling to a certain degree without accompanying deleterious effects on plant morphology, but in sorghum, it leads to abnormal culm bending 18 . This led to a conundrum in sorghum because reducing plant height by severely modifying other mechanisms often leads to negative side effects in plants.…”

Section: Discussionmentioning

confidence: 99%

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

Hirano

Kawamura

Araki-Nakamura

et al. 2017

Sci Rep

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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...

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“…Compared to other energy crops, such as sugar cane, sorghum requires less fertilizer and water, and has similar annual productivity per acre (Kim and Day, 2011). In addition, molecular genetic engineering techniques for the breeding of sorghum have also been established (Ordonio et al, 2014). For these reasons, the utilization of sorghum for biofuel production has been intensively investigated (Matsakas and Christakopoulos, 2013;Wang et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Phenyllactic acid production by simultaneous saccharification and fermentation of pretreated sorghum bagasse

Kawaguchi

Teramura

Uematsu

et al. 2015

Bioresource Technology

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Gibberellin deficiency pleiotropically induces culm bending in sorghum: an insight into sorghum semi-dwarf breeding

Cited by 41 publications

References 59 publications

Mapping of a Cellulose-Deficient Mutant Named dwarf1-1 in Sorghum bicolor to the Green Revolution Gene gibberellin20-oxidase Reveals a Positive Regulatory Association between Gibberellin and Cellulose Biosynthesis

Mapping of a Cellulose-Deficient Mutant Named dwarf1-1 in Sorghum bicolor to the Green Revolution Gene gibberellin20-oxidase Reveals a Positive Regulatory Association between Gibberellin and Cellulose Biosynthesis

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

Phenyllactic acid production by simultaneous saccharification and fermentation of pretreated sorghum bagasse

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