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
Masaki Okamura A , Tatsuro Hirose A B , Yoichi Hashida A , Tohru Yamagishi A , Ryu Ohsugi A and Naohiro Aoki A CA 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 40(11) 1137-1146 https://doi.org/10.1071/FP13105
Submitted: 19 April 2013 Accepted: 17 May 2013 Published: 21 June 2013
Abstract
Starch accumulated in rice (Oryza sativa L.) stems before heading as nonstructural carbohydrates (NSCs) is reported to be important for improving and stabilising grain yield. To evaluate the importance of stem starch, we investigated a retrotransposon (Tos17) insertion rice mutant lacking a gene encoding a large subunit of ADP-glucose pyrophosphorylase (AGP) called OsAGPL1 or OsAPL3. The AGP activity and starch contents of the mutant were drastically reduced in the stem (i.e. leaf sheath and culm) but not in the leaf blade or endosperm. This starch reduction in the leaf sheaths of the mutant was complemented by the introduction of wild-type OsAGPL1. These results strongly suggest that OsAGPL1 plays a principal role in stem starch accumulation. Field experimentations spanning 2 years revealed that the mutant plants were shorter than the wild-type plants. Moreover, the tiller number and angle were larger in the mutant plants than the wild-type plants, but the dry weight at heading stage was not different. The grain yield was slightly lower in control plots without shading treatment. However, this difference increased substantially with shading. Therefore, stem starch is indispensable for normal ripening under low irradiance conditions and probably contributes to the maintenance of appropriate plant architecture.
Additional keywords: nonstructural carbohydrate, shading, stem starch, tiller angle, tiller number.
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=e9ae910f735a238184aa072a9bd4e9f2CAS |
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=88dae88320409df314fed5647f08a102CAS |
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=3de8e5fac0d540bb5b9ad2359342d0fdCAS |
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=1c812d00da61c6bc9a409b7fe92ed62fCAS | 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=f58000b3b0cb3208c50e83bba9e58cfeCAS |
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=c4e578a3af71ecfef7bfdbd94997e76dCAS | 11539053PubMed |
Kuroda M, Kimizu M, Mikami C (2010) A simple set of plasmids for the production of transgenic plants. Bioscience, Biotechnology, and Biochemistry 74, 2348–2351.
| A simple set of plasmids for the production of transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGgu73O&md5=30b485cb4bd9b7065edb9edc728aaedeCAS | 21071849PubMed |
Lee S, Hwang S, Han M, Eom J, Kang H, Han Y, Choi S, Cho M, Bhoo SH, An G, Hahn T, Okita TW, Jeon J (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Molecular Biology 65, 531–546.
| Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2itbfL&md5=8b13ee9c8ac1f3705cb44aaa32fd2ca4CAS | 17406793PubMed |
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=edad24f3f6282c43cb71dc9e637c72c3CAS | 17468779PubMed |
Loreti E, Alpi A, Perata P (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of α-amylase in barley embryos. Plant Physiology 123, 939–948.
| Glucose and disaccharide-sensing mechanisms modulate the expression of α-amylase in barley embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1SlsbY%3D&md5=56b9ea6fcca8af2aaf83341592ba6e75CAS | 10889242PubMed |
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 |
Nagata K, Yoshinaga S, Takanashi J, Terao T (2001) Effects of dry matter production, translocation of nonstructural carbohydrates and nitrogen application on grain filling in rice cultivar Takanari, a cultivar bearing a large number of spikelets. Plant Production Science 4, 173–183.
| Effects of dry matter production, translocation of nonstructural carbohydrates and nitrogen application on grain filling in rice cultivar Takanari, a cultivar bearing a large number of spikelets.Crossref | GoogleScholarGoogle Scholar |
Nakamura Y, Yuki K, Park S, Ohya T (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant & Cell Physiology 30, 833–839.
Ohdan T, Francisco P, 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=7cd8d9a22e2de1253d90908d573afce2CAS | 16275672PubMed |
Okamura M, Aoki N, Hirose T, Yonekura M, Ohto C, Ohsugi R (2011) Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice. Plant Science 181, 159–166.
| Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslKnt7w%3D&md5=b1675b61193ddc4a3ffe9b873934cf86CAS | 21683881PubMed |
Pan J, Cui K, Wei D, Huang J, Xiang J, Nie L (2011) Relationships of non-structural carbohydrates accumulation and translocation with yield formation in rice recombinant inbred lines under two nitrogen levels. Physiologia Plantarum 141, 321–331.
| Relationships of non-structural carbohydrates accumulation and translocation with yield formation in rice recombinant inbred lines under two nitrogen levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktlars7k%3D&md5=cdcee272c9da8883b9d8f1c17bc18a07CAS | 21175644PubMed |
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Physiology 57, 675–709.
| Sugar sensing and signaling in plants: conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7k%3D&md5=51c252f22fd5eba6aecaf76c949f2ee7CAS |
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 |
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=e31d8a5aca7d14ebb710a0062928dda2CAS | 22732107PubMed |
Soga Y, Nozaki M (1957) Studies on the relation between seasonal changes of carbohydrates accumulated and the ripening at the stage of generative growth in rice plant. Japanese Journal of Crop Science 26, 105–108.
| Studies on the relation between seasonal changes of carbohydrates accumulated and the ripening at the stage of generative growth in rice plant.Crossref | GoogleScholarGoogle Scholar |
Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany 55, 2131–2145.
| Recent developments in understanding the regulation of starch metabolism in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVOkt70%3D&md5=f27ee120799dd44055e69a3f02ee1432CAS | 15361536PubMed |
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. The Plant Journal 47, 969–976.
| Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsL%2FE&md5=ed53b3e954025e4c295097e218f33b87CAS | 16961734PubMed |
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=da5a46a12d8a8ee56350b95029703a48CAS | 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=f6db82340162ceadeaac2432a26c0947CAS | 11542271PubMed |
Wenzler H, Mignery G, Fisher L, Park W (1989) Sucrose-regulated expression of a chimeric potato tuber gene in leaves of transgenic tobacco plants. Plant Molecular Biology 13, 347–354.
| Sucrose-regulated expression of a chimeric potato tuber gene in leaves of transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXjtlequw%3D%3D&md5=e9fc792faf28d76aa5afea3ea73a225dCAS | 2491661PubMed |
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=c094184590274a249fb915946aaa4605CAS | 23124325PubMed |
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=005c34c0b9ea83709a6b3cd1a3e62323CAS | 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=580efeb25fe053243e676536982b36eeCAS |
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=ad70703330a19dbedc3f7342e04352d7CAS | 17908158PubMed |