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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Suppression of starch synthesis in rice stems splays tiller angle due to gravitropic insensitivity but does not affect yield

Masaki Okamura A , Tatsuro Hirose A B , Yoichi Hashida A , Ryu Ohsugi A and Naohiro Aoki A C
+ Author Affiliations
- Author Affiliations

A Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, 113-8657, Japan.

B NARO Agricultural Research Center, Joetsu, Niigata 943-0193, Japan.

C Corresponding author. Email: aaokin@mail.ecc.u-tokyo.ac.jp

Functional Plant Biology 42(1) 31-41 https://doi.org/10.1071/FP14159
Submitted: 12 June 2014  Accepted: 11 July 2014   Published: 17 September 2014

Abstract

In rice (Oryza sativa L.), tiller angle – defined as the angle between the main culm and its side tillers – is one of the important factors involved in light use efficiency. To clarify the relationship between tiller angle, gravitropism and stem-starch accumulation, we investigated the shoot gravitropic response of a low stem-starch rice mutant which lacks a large subunit of ADP-glucose pyrophosphorylase (AGP), called OsAGPL1 and exhibits relatively spread tiller angle. The insensitive gravitropic response exhibited by the mutant led us to the conclusion that insensitivity of gravitropism caused by stem-starch reduction splayed the tiller angle. Furthermore, since another AGP gene called OsAGPL3 was expressed at considerable levels in graviresponding sites, we generated a double mutant lacking both OsAGPL1 and OsAGPL3. The double mutant exhibited still lower stem-starch content, less sensitive gravitropic response and greater tiller angle spread than the single mutants. This indicated that the expansion of the tiller angle caused by the reduction in starch level was intense according to the extent of the reduction. We found there were no significant differences between the double mutant and wild-type plants in terms of dry matter production. These results provided new insight into the importance of stem-starch accumulation and ideal plant architecture.

Additional keywords: gravitropism, leaf sheath pulivinus, non-structural carbohydrate, plant architecture, stem starch.


References

Abe K, Suge H (1993) Role of gravitropic response in the dry-matter production of rice (Oryza sativa L.): An experiment with a line having lazy gene. Journal of Plant Research 106, 337–343.
Role of gravitropic response in the dry-matter production of rice (Oryza sativa L.): An experiment with a line having lazy gene.Crossref | GoogleScholarGoogle Scholar |

Akihiro T, Mizuno K, Fujimura T (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant & Cell Physiology 46, 937–946.
Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslCht74%3D&md5=74e4386d77d0ea3b00bf9d1b9a804f53CAS |

Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L) deficient in chloroplast phosphoglucomutase activity. Plant Physiology 79, 11–17.
Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L) deficient in chloroplast phosphoglucomutase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFehs74%3D&md5=6641707c3147046b6dfebf512ae6ea5dCAS | 16664354PubMed |

Caspar T, Lin T, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiology 95, 1181–1188.
Mutants of Arabidopsis with altered regulation of starch degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVCgsLw%3D&md5=5dac6b553ddfe736d4427bbe89df46faCAS | 16668109PubMed |

Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113–116.
A simple and efficient method for isolating RNA from pine trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslKqurs%3D&md5=248b8f072333e8085cf42717fe9e4d3aCAS |

Chen Y, Fan X, Song W, Zhang Y, Xu G (2012) Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnology Journal 10, 139–149.
Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Wksrs%3D&md5=262068fdeafd64e50b3cb2588f705775CAS | 21777365PubMed |

Cook FR, Fahy B, Trafford K (2012) A rice mutant lacking a large subunit of ADP-glucose pyrophosphorylase has drastically reduced starch content in the culm but normal plant morphology and yield. Functional Plant Biology 39, 1068–1078.
A rice mutant lacking a large subunit of ADP-glucose pyrophosphorylase has drastically reduced starch content in the culm but normal plant morphology and yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKru7%2FO&md5=465693a9ff4fb20ca4528c0fcebd01fdCAS |

Hashiguchi Y, Tasaka M, Morita MT (2013) Mechanism of higher plant gravity sensing. American Journal of Botany 100, 91–100.
Mechanism of higher plant gravity sensing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKltbc%3D&md5=43941d9723d481cf8497df00235864fbCAS | 23115136PubMed |

Hirose T, Ohdan T, Nakamura Y, Terao T (2006) Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiologia Plantarum 128, 425–435.
Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Grt73I&md5=4aa8513a8769755bfa19451b788bc707CAS |

Hirose T, Aoki N, Harada Y, Okamura M, Hashida Y, Ohsugi R, Miyao A, Hirochika H, Terao T (2013) Disruption of a rice gene for α-glucan water dikinase, OsGWD1, leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth. Frontiers in Plant Science 4, 147
Disruption of a rice gene for α-glucan water dikinase, OsGWD1, leads to hyperaccumulation of starch in leaves but exhibits limited effects on growth.Crossref | GoogleScholarGoogle Scholar | 23750161PubMed |

Huber SC, Hanson KR (1992) Carbon partitioning and growth of a starchless mutant of Nicotiana sylvestris. Plant Physiology 99, 1449–1454.
Carbon partitioning and growth of a starchless mutant of Nicotiana sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVynsrc%3D&md5=e3041103f05e550ec120655a0f34e3c3CAS | 16669057PubMed |

Huber SC, Huber JA, Hanson KR (1990) Regulation of the partitioning of products of photosynthesis. In ‘The perspectives in biochemical and genetic regulation of photosynthesis’. pp. 85–101 (Wiley-Liss: New York)

Jeon J, Jung K, Kim H, Suh J, Khush GS (2011) Genetic and molecular insights into the enhancement of rice yield potential. Journal of Plant Biology 54, 1–9.
Genetic and molecular insights into the enhancement of rice yield potential.Crossref | GoogleScholarGoogle Scholar |

Kaufman PB, Brock TG, Song I, Rho Y, Ghosheh NS (1987) How cereal grass shoots perceive and respond to gravity. American Journal of Botany 74, 1446–1457.
How cereal grass shoots perceive and respond to gravity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnlslKitw%3D%3D&md5=c2b0ae669016237dfff73c809486183aCAS | 11539053PubMed |

Li P, Wang Y, Qian Q, Fu Z, Wang M, Zeng D, Li B, Wang X, Li J (2007) LAZY1 controls rice shoot gravitropism through regulating polar auxin transport. Cell Research 17, 402–410.
LAZY1 controls rice shoot gravitropism through regulating polar auxin transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Wktbg%3D&md5=6754448fff8ddac01b0c61f8579d0d70CAS | 17468779PubMed |

Lin T, Caspar T, Somerville C, Preiss J (1988) Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L) Heynh. lacking ADP glucose pyrophosphorylase activity. Plant Physiology 86, 1131–1135.
Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L) Heynh. lacking ADP glucose pyrophosphorylase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkt1SgtL0%3D&md5=c5b65f205e34401b8f489672ee36c0b3CAS | 16666044PubMed |

Maeda E (1960) Geotropic reaction of excised rice leaves. Physiologia Plantarum 13, 204–213.
Geotropic reaction of excised rice leaves.Crossref | GoogleScholarGoogle Scholar |

Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. The Plant Cell 15, 1771–1780.
Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome.Crossref | GoogleScholarGoogle Scholar | 12897251PubMed |

Ohdan T, Francisco PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany 56, 3229–3244.
Expression profiling of genes involved in starch synthesis in sink and source organs of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GlsbnJ&md5=8d0cdaa96a46c3d5839c2ec76d1e40a7CAS | 16275672PubMed |

Okamura M, Hirose T, Hashida Y, Yamagishi T, Ohsugi R, Aoki N (2013) Starch reduction in rice stems due to a lack of OsAGPL1 or OsAPL3 decreases grain yield under low irradiance during ripening and modifies plant architecture. Functional Plant Biology 40, 1137–1146.
Starch reduction in rice stems due to a lack of OsAGPL1 or OsAPL3 decreases grain yield under low irradiance during ripening and modifies plant architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1eqsrrI&md5=45c616d7a806e7c7e1669a0acf492e80CAS |

Ragel P, Streb S, Feil R, Sahrawy M, Annunziata MG, Lunn JE, Zeeman S, Mérida Á (2013) Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiology 163, 75–85.
Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVygsbvP&md5=297b47f81972b58e2c2f940593c666aeCAS | 23872660PubMed |

Rösti S, Fahy B, Denyer K (2007) A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally. Functional Plant Biology 34, 480–489.
A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally.Crossref | GoogleScholarGoogle Scholar |

Sakamoto T, Morinaka Y, Ohnishi T, Sunohara H, Fujioka S, Ueguchi-Tanaka M, Mizutani M, Sakata K, Takatsuto S, Yoshida S, Tanaka H, Kitano H, Matsuoka M (2006) Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nature Biotechnology 24, 105–109.
Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisVGksg%3D%3D&md5=f7560b8103fc348141e63ee748644277CAS | 16369540PubMed |

Slewinski TL (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. Journal of Experimental Botany 63, 4647–4670.
Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Kjsb7J&md5=aa61556222b17f2b76f9931c93ce850bCAS | 22732107PubMed |

Song Y, Xu Z (2013) Ectopic overexpression of an AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) gene OsIAA4 in rice induces morphological changes and reduces responsiveness to auxin. International Journal of Molecular Sciences 14, 13645–13656.
Ectopic overexpression of an AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) gene OsIAA4 in rice induces morphological changes and reduces responsiveness to auxin.Crossref | GoogleScholarGoogle Scholar | 23812082PubMed |

Song Q, Zhang G, Zhu X (2013) Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2 – a theoretical study using a mechanistic model of canopy photosynthesis. Functional Plant Biology 40, 108–124.
Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2 – a theoretical study using a mechanistic model of canopy photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Knu74%3D&md5=3497af8e71c56ef135a61dd614ae3920CAS |

Tanimoto M, Tremblay R, Colasanti J (2008) Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropism 5 mutant are associated with reduced starch levels. Plant Molecular Biology 67, 57–69.
Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropism 5 mutant are associated with reduced starch levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1KrtL8%3D&md5=76b324345659e75591f5e71b4041410dCAS | 18259878PubMed |

Vriet C, Welham T, Brachmann A, Pike M, Pike J, Perry J, Parniske M, Sato S, Tabata S, Smith AM, Wang TL (2010) A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism. Plant Physiology 154, 643–655.
A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCkt7vJ&md5=6b56d9dab29891eda70dc6bc1158db11CAS | 20699404PubMed |

Wang J, Jiang J, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Science 156, 201–211.
Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjtr0%3D&md5=8551945feda6a08f7ad93a021494b687CAS | 10936527PubMed |

Weise SE, Kiss JZ (1999) Gravitropism of inflorescence stems in starch-deficient mutants of Arabidopsis. International Journal of Plant Sciences 160, 521–527.
Gravitropism of inflorescence stems in starch-deficient mutants of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnmtVynsQ%3D%3D&md5=480968d4fc796975454e8554aec705bfCAS | 11542271PubMed |

Wu X, Tang D, Li M, Wang K, Cheng Z (2013) Loose Plant Architecture1, an INDETERMINATE DOMAIN protein involved in shoot gravitropism, regulates plant architecture in rice. Plant Physiology 161, 317–329.
Loose Plant Architecture1, an INDETERMINATE DOMAIN protein involved in shoot gravitropism, regulates plant architecture in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVCksro%3D&md5=68fe439b04c21b55043f3d794a7c56feCAS | 23124325PubMed |

Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant & Cell Physiology 46, 1674–1681.
A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1SltL3O&md5=d5fe426a52bbe0664ec6ca22d07597feCAS |

Yang X, Hwa C (2008) Genetic modification of plant architecture and variety improvement in rice. Heredity 101, 396–404.
Genetic modification of plant architecture and variety improvement in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Krtb7M&md5=15c89ddfa9684f00ff81f61f354c73d9CAS | 18716608PubMed |

Yoshida S (1972) Physiological aspects of grain yield. Annual Review of Plant Physiology 23, 437–464.
Physiological aspects of grain yield.Crossref | GoogleScholarGoogle Scholar |

Yoshihara T, Iino M (2007) Identification of the gravitropism-related rice gene LAZY1 and elucidation of LAZY1-dependent and -independent gravity signaling pathways. Plant & Cell Physiology 48, 678–688.
Identification of the gravitropism-related rice gene LAZY1 and elucidation of LAZY1-dependent and -independent gravity signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmslyiuro%3D&md5=9ea81bfd0dcae7d723b1d1a37de1236dCAS |

Yu B, Lin Z, Li H, Li X, Li J, Wang Y, Zhang X, Zhu Z, Zhai W, Wang X, Xie D, Sun C (2007) TAC1, a major quantitative trait locus controlling tiller angle in rice. The Plant Journal 52, 891–898.
TAC1, a major quantitative trait locus controlling tiller angle in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVGlsrfJ&md5=f04e0c3e3abf01549c62c0cc41cf5918CAS | 17908158PubMed |