Production and roles of IAA and ABA during development of superior and inferior rice grains
Heather M. Nonhebel A C and Karina Griffin A BA School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.
B Present address: Macadamia Processing Company, 2 Cowlong Road, Lindendale NSW 2480, Australia.
C Corresponding author. Email: hnonheb2@une.edu.au
Functional Plant Biology 47(8) 716-726 https://doi.org/10.1071/FP19291
Submitted: 9 October 2019 Accepted: 10 February 2020 Published: 22 May 2020
Abstract
Current understanding of the role of plant hormones during cereal grain filling is confounded by contradictory reports on hormone production that is based on poor methodology. We report here on the accurate measurement of indole-3-acetic acid (IAA) and abscisic acid (ABA) by combined liquid chromatography-tandem mass spectrometry in multiple reaction-monitoring mode with heavy isotope labelled internal standards. ABA and IAA contents of superior versus inferior rice grains (ABA maxima 159 ng g–1 FW and 109 ng g–1 FW, IAA maxima 2 µg g–1 FW and 1.7 µg g–1 FW respectively) correlated with the expression of biosynthetic genes and with grain fill. Results confirm that grain ABA is produced primarily by OsNCED2(5), but suggest that ABA import and metabolism also play important roles in ABA regulation. The IAA content of grains is primarily influenced by OsYUC9 and OsYUC11. However, the distinct expression profile of OsYUC12 suggests a specific role for IAA produced by this enzyme. Co-expression of OsYUC12 with OsIAA29 indicates their involvement in a common signalling pathway. Co-expression and cis-element analysis identified several aleurone-specific transcriptional regulators as well as glutelin as strong candidates for detailed investigation for direct regulation by the auxin-signalling pathway.
Additional keywords: cereal grain fill, dorsal aleurone, endosperm, MRP-1, Oryza sativa, OsNF-YC, RISBZ1.
References
Abu-Zaitoon YM, Bennett K, Normanly J, Nonhebel HM (2012) A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA. Physiologia Plantarum 146, 487–499.| A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA.Crossref | GoogleScholarGoogle Scholar | 22582989PubMed |
Aoki K, Ogata Y, Shibata D (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant & Cell Physiology 48, 381–390.
| Approaches for extracting practical information from gene co-expression networks in plant biology.Crossref | GoogleScholarGoogle Scholar |
Barkawi LS, Tam YY, Tillman JA, Pederson B, Calio J, Al-Amier H, Emerick M, Normanly J, Cohen JD (2008) A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue. Analytical Biochemistry 372, 177–188.
| A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue.Crossref | GoogleScholarGoogle Scholar | 17889819PubMed |
Bello BK, Hou Y, Zhao J, Jiao G, Wu Y, Li Z, Wang Y, Tong X, Wang W, Yuan W, Wei X, Zhang J (2019) NF-YB1-YC12-bHLH144 complex directly activates Wx to regulate grain quality in rice (Oryza sativa L.). Plant Biotechnology Journal 17, 1222–1235.
| NF-YB1-YC12-bHLH144 complex directly activates Wx to regulate grain quality in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 30552799PubMed |
Berendzen KW, Weiste C, Wanke D, Kilian J, Harter K, Droge-Laser W (2012) Bioinformatic cis-element analyses performed in Arabidopsis and rice disclose bZIP- and MYB-related binding sites as potential AuxRE-coupling elements in auxin-mediated transcription. BMC Plant Biology 12, 125
| Bioinformatic cis-element analyses performed in Arabidopsis and rice disclose bZIP- and MYB-related binding sites as potential AuxRE-coupling elements in auxin-mediated transcription.Crossref | GoogleScholarGoogle Scholar | 22852874PubMed |
Bernardi J, Lanubile A, Li Q-B, Kumar D, Kladnik A, Cook SD, Ross JJ, Marocco A, Chourey PS (2012) Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiology 160, 1318–1328.
| Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize.Crossref | GoogleScholarGoogle Scholar | 22961134PubMed |
Bernardi J, Li QB, Gao Y, Zhao Y, Battaglia R, Marocco A, Chourey PS (2016) The auxin-deficient defective kernel18 (dek18) mutation alters the expression of seed-specific biosynthetic genes in maize. Journal of Plant Growth Regulation 35, 770–777.
| The auxin-deficient defective kernel18 (dek18) mutation alters the expression of seed-specific biosynthetic genes in maize.Crossref | GoogleScholarGoogle Scholar |
Bernardi J, Battaglia R, Bagnaresi P, Lucini L, Marocco A (2019) Transcriptomic and metabolomic analysis of ZmYUC1 mutant reveals the role of auxin during early endosperm formation in maize. Plant Science 281, 133–145.
| Transcriptomic and metabolomic analysis of ZmYUC1 mutant reveals the role of auxin during early endosperm formation in maize.Crossref | GoogleScholarGoogle Scholar | 30824046PubMed |
Bruno M, Koschmieder J, Wuest F, Schaub P, Fehling-Kaschek M, Timmer J, Beyer P, Al-Babili S, Hancock R (2016) Enzymatic study on AtCCD4 and AtCCD7 and their potential to form acyclic regulatory metabolites. Journal of Experimental Botany 67, 5993–6005.
| Enzymatic study on AtCCD4 and AtCCD7 and their potential to form acyclic regulatory metabolites.Crossref | GoogleScholarGoogle Scholar | 27811075PubMed |
Chen K-H, Miller AN, Patterson GW, Cohen JD (1988) A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis. Plant Physiology 86, 822–825.
| A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis.Crossref | GoogleScholarGoogle Scholar | 16665995PubMed |
Cheng WH, Taliercio EW, Chourey PS (1996) The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. The Plant Cell 8, 971–983.
| The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel.Crossref | GoogleScholarGoogle Scholar | 12239408PubMed |
Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA (2011) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Research 40, D1194–D1201.
| PLEXdb: gene expression resources for plants and plant pathogens.Crossref | GoogleScholarGoogle Scholar | 22084198PubMed |
Diaz I, Vicente-Carbajosa J, Abraham Z, Martinez M, Isabel-La Moneda I, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. The Plant Journal 29, 453–464.
| The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development.Crossref | GoogleScholarGoogle Scholar | 11846878PubMed |
Doll NM, Depege-Fargeix N, Rogowsky PM, Widiez T (2017) Signaling in early maize kernel development. Molecular Plant 10, 375–388.
| Signaling in early maize kernel development.Crossref | GoogleScholarGoogle Scholar | 28267956PubMed |
Fu J, Xu Y, Chen L, Yuan L, Wang Z, Yang J (2013) Changes in enzyme activities involved in starch synthesis and hormone concentrations in superior and inferior spikelets and their association with grain filling of super rice. Rice Science 20, 120–128.
| Changes in enzyme activities involved in starch synthesis and hormone concentrations in superior and inferior spikelets and their association with grain filling of super rice.Crossref | GoogleScholarGoogle Scholar |
Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M, Kato H, Kikuchi S, Hamada K, Mochizuki T, Ishimizu T, Iwai H, Tsutsumi N, Kurata N (2010) Rice expression atlas in reproductive development. Plant & Cell Physiology 51, 2060–2081.
| Rice expression atlas in reproductive development.Crossref | GoogleScholarGoogle Scholar |
Gómez E, Royo J, Guo Y, Thompson R, Hueros G (2002) Establishment of cereal endosperm expression domains identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. The Plant Cell 14, 599–610.
| Establishment of cereal endosperm expression domains identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1.Crossref | GoogleScholarGoogle Scholar | 11910007PubMed |
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186.
| Phytozome: a comparative platform for green plant genomics.Crossref | GoogleScholarGoogle Scholar | 22110026PubMed |
Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. The Plant Cell 7, 1879–1891.
Guo T, Chen K, Dong NQ, Ye WW, Shan JX, Lin HX (2019) Tillering and small grain 1 dominates the tryptophan aminotransferase family required for local auxin biosynthesis in rice. Journal of Integrative Plant Biology
| Tillering and small grain 1 dominates the tryptophan aminotransferase family required for local auxin biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 31081210PubMed |
Hirai N, Kondo S, Ohigashi H (2003) Deuterium-labeled phaseic acid and dihydrophaseic acids for internal standards. Bioscience, Biotechnology, and Biochemistry 67, 2408–2415.
| Deuterium-labeled phaseic acid and dihydrophaseic acids for internal standards.Crossref | GoogleScholarGoogle Scholar | 14646201PubMed |
Huang Y, Guo Y, Liu Y, Zhang F, Wang Z, Wang H, Wang F, Li D, Mao D, Luan S, Liang M, Chan L (2018) 9-cis-Epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Frontiers of Plant Science 9, 162
| 9-cis-Epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
Huang Y, Jiao Y, Xie N, Guo Y, Zhang F, Xiang Z, Wang R, Wang F, Gao Q, Tian L, Li D, Chen L, Liang M (2019) OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Science 287, 110188
| OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice.Crossref | GoogleScholarGoogle Scholar | 31481229PubMed |
Hwang SG, Chen HC, Huang WY, Chu YC, Shii CT, Cheng WH (2010) Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. Plant Science 178, 12–22.
| Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology.Crossref | GoogleScholarGoogle Scholar |
Hwang S-G, Lee C-Y, Tseng C-S (2018) Heterologous expression of rice 9-cis-epoxycarotenoid dioxygenase 4 (OsNCED4) in Arabidopsis confers sugar oversensitivity and drought tolerance. Botanical Studies 59, 2
| Heterologous expression of rice 9-cis-epoxycarotenoid dioxygenase 4 (OsNCED4) in Arabidopsis confers sugar oversensitivity and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 29335785PubMed |
Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiology 143, 1467–1483.
| F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 17293439PubMed |
Jiang D, Chen W, Dong J, Li J, Yang F, Wu Z, Zhou H, Wang W, Zhuang C (2018) Overexpression of miR164b-resistant OsNAC2 improves plant architecture and grain yield in rice. Journal of Experimental Botany 69, 1533–1543.
| Overexpression of miR164b-resistant OsNAC2 improves plant architecture and grain yield in rice.Crossref | GoogleScholarGoogle Scholar | 29365136PubMed |
Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant & Cell Physiology 51, 1988–2001.
| Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions.Crossref | GoogleScholarGoogle Scholar |
Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6, 4
| Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data.Crossref | GoogleScholarGoogle Scholar | 24280374PubMed |
Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. The Plant Journal 59, 908–920.
| Compensation and interaction between RISBZ1 and RPBF during grain filling in rice.Crossref | GoogleScholarGoogle Scholar | 19473328PubMed |
Kuwano M, Masumura T, Yoshida KT (2011) A novel endosperm transfer cell-containing region-specific gene and its promoter in rice. Plant Molecular Biology 76, 47–56.
| A novel endosperm transfer cell-containing region-specific gene and its promoter in rice.Crossref | GoogleScholarGoogle Scholar | 21409497PubMed |
LeClere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiology 153, 306–318.
| Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels.Crossref | GoogleScholarGoogle Scholar | 20237017PubMed |
Li MN, Xu WY, Yang WQ, Kong ZS, Xue YB (2007) Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice. Plant Physiology 144, 1797–1812.
| Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice.Crossref | GoogleScholarGoogle Scholar |
Li M, Singh R, Bazanova N, Milligan AS, Shirley N, Langridge P, Lopato S (2008) Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley. Plant Biotechnology Journal 6, 465–476.
| Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley.Crossref | GoogleScholarGoogle Scholar | 18422887PubMed |
Li QF, Sun SSM, Yuan DY, Yu HX, Gu MH, Liu QQ (2010) Validation of candidate reference genes for the accurate normalization of real-time quantitative RT-PCR data in rice during seed development. Plant Molecular Biology Reporter 28, 49–57.
| Validation of candidate reference genes for the accurate normalization of real-time quantitative RT-PCR data in rice during seed development.Crossref | GoogleScholarGoogle Scholar |
Magnard JL, Lehouque G, Massonneau AE, Frangne N, Heckel T, Gutierrez-Marcos JF, Perez P, Dumas C, Rogowsky PM (2003) ZmEBE genes show a novel, continuous expression pattern in the central cell before fertilization and in specific domains of the resulting endosperm after fertilization. Plant Molecular Biology 53, 821–836.
| ZmEBE genes show a novel, continuous expression pattern in the central cell before fertilization and in specific domains of the resulting endosperm after fertilization.Crossref | GoogleScholarGoogle Scholar | 15082928PubMed |
Mathew IE, Das S, Mahto A, Agarwal P (2016) Three rice NAC transcription factors heteromerize and are associated with seed size. Frontiers of Plant Science 7, 638
| Three rice NAC transcription factors heteromerize and are associated with seed size.Crossref | GoogleScholarGoogle Scholar |
McAdam EL, Meitzel T, Quittenden LJ, Davidson SE, Dalmais M, Bendahmane AI, Thompson R, Smith JJ, Nichols DS, Urquhart S, Gelinas-Marion A, Aubert G, Ross JJ (2017) Evidence that auxin is required for normal seed size and starch synthesis in pea. New Phytologist 216, 193–204.
| Evidence that auxin is required for normal seed size and starch synthesis in pea.Crossref | GoogleScholarGoogle Scholar | 28748561PubMed |
Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid JB, Gubler F (2006) Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8′-hydroxylase. The Plant Journal 45, 942–954.
| Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8′-hydroxylase.Crossref | GoogleScholarGoogle Scholar | 16507085PubMed |
Onodera Y, Suzuki A, Wu CY, Washida H, Takaiwa F (2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. Journal of Biological Chemistry 276, 14139–14152.
| A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif.Crossref | GoogleScholarGoogle Scholar | 11133985PubMed |
Rubio-Somoza I, Martinez M, Abraham Z, Diaz I, Carbonero P (2006) Ternary complex formation between HvMYBS3 and other factors involved in transcriptional control in barley seeds. The Plant Journal 47, 269–281.
| Ternary complex formation between HvMYBS3 and other factors involved in transcriptional control in barley seeds.Crossref | GoogleScholarGoogle Scholar | 16762033PubMed |
Russell French S, Abu-Zaitoon Y, Uddin M, Bennett K, Nonhebel H (2014) Auxin and cell wall invertase related signaling during rice grain development. Plants 3, 95–112.
| Auxin and cell wall invertase related signaling during rice grain development.Crossref | GoogleScholarGoogle Scholar |
Sato Y, Namiki N, Takehisa H, Kamatsuki K, Minami H, Ikawa H, Ohyanagi H, Sugimoto K, Itoh JI, Antonio BA, Nagamura Y (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Research 41, D1214–D1221.
| RiceFREND: a platform for retrieving coexpressed gene networks in rice.Crossref | GoogleScholarGoogle Scholar | 23180784PubMed |
Schreiber B (2014) Signalling and nutrient partitioning during sorghum grain fill. Bachelor of Science Honours thesis. School of Science and Technology, The University of New England, Armidale, NSW, Australia.
Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, Scholz U, Wobus U, Sreenivasulu N (2011) ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. Journal of Experimental Botany 62, 2615–2632.
| ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions.Crossref | GoogleScholarGoogle Scholar | 21289079PubMed |
Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. Journal of Experimental Botany 53, 947–958.
| Cereal seed storage proteins: structures, properties and role in grain utilization.Crossref | GoogleScholarGoogle Scholar | 11912237PubMed |
Stelpflug SC, Sekhon RS, Vaillancourt B, Hirsch CN, Buell CR, de Leon N, Kaeppler SM (2016) An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development. The Plant Genome 9, 1–16.
| An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development.Crossref | GoogleScholarGoogle Scholar |
Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal 35, 44–56.
| Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family.Crossref | GoogleScholarGoogle Scholar | 12834401PubMed |
Tang T, Xie H, Wang YX, Lu B, Liang JS (2009) The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.). Journal of Experimental Botany 60, 2641–2652.
| The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 19401410PubMed |
Taylor IB, Sonneveld T, Bugg TDH, Thompson AJ (2005) Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. Journal of Plant Growth Regulation 24, 253–273.
Walcher CL, Nemhauser JL (2012) Bipartite promoter element required for auxin response. Plant Physiology 158, 273–282.
| Bipartite promoter element required for auxin response.Crossref | GoogleScholarGoogle Scholar | 22100645PubMed |
Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. Journal of Experimental Botany 64, 3453–3466.
| OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm.Crossref | GoogleScholarGoogle Scholar | 23846875PubMed |
Wang Z, Xu Y, Chen T, Zhang H, Yang J, Zhang J (2015) Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta 241, 1091–1107.
| Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling.Crossref | GoogleScholarGoogle Scholar | 25589060PubMed |
Wang G-Q, Li H-X, Feng L, Chen M-X, Meng S, Ye N-H, Zhang J (2019) Transcriptomic analysis of grain filling in rice inferior grains under moderate soil drying. Journal of Experimental Botany 70, 1597–1611.
| Transcriptomic analysis of grain filling in rice inferior grains under moderate soil drying.Crossref | GoogleScholarGoogle Scholar | 30690492PubMed |
Wu C, Washida H, Onodera Y, Harada K, Takaiwa F (2000) Quantitative nature of the prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. The Plant Journal 23, 415–421.
| Quantitative nature of the prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression.Crossref | GoogleScholarGoogle Scholar | 10929134PubMed |
Wu X, Liu J, Li D, Liu C-M (2016) Rice caryopsis development II: Dynamic changes in the endosperm. Journal of Integrative Plant Biology 58, 786–798.
| Rice caryopsis development II: Dynamic changes in the endosperm.Crossref | GoogleScholarGoogle Scholar | 27449987PubMed |
Xu J-J, Zhang X-F, Xue H-W (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. Journal of Experimental Botany 67, 6399–6411.
| Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor.Crossref | GoogleScholarGoogle Scholar | 27803124PubMed |
Yamamoto MP, Onodera Y, Touno SM, Takaiwa F (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiology 141, 1694–1707.
| Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes.Crossref | GoogleScholarGoogle Scholar | 16798940PubMed |
Yang J, Zhang J (2010) Grain-filling problem in ‘super’ rice. Journal of Experimental Botany 61, 1–5.
| Grain-filling problem in ‘super’ rice.Crossref | GoogleScholarGoogle Scholar | 19959608PubMed |
You CC, Zhu HL, Xu BB, Huang W, Wang S, Ding Y, Liu Z, Li G, Chen L, Ding CQ, Tang S (2016) Effect of removing superior spikelets on grain filling of inferior spikelets in rice. Frontiers of Plant Science 7, 1161
| Effect of removing superior spikelets on grain filling of inferior spikelets in rice.Crossref | GoogleScholarGoogle Scholar |
Zemlyanskaya EV, Wiebe DS, Omelyanchuk NA, Levitsky VG, Mironova VV (2016) Meta-analysis of transcriptome data identified TGTCNN motif variants associated with the response to plant hormone auxin in Arabidopsis thaliana L. Journal of Bioinformatics and Computational Biology 14, 1641009
| Meta-analysis of transcriptome data identified TGTCNN motif variants associated with the response to plant hormone auxin in Arabidopsis thaliana L.Crossref | GoogleScholarGoogle Scholar | 27122321PubMed |
Zhang H, Tan GLL, Yang LNN, Yang JC, Zhang JH, Zhao BH (2009) Hormones in the grains and roots in relation to post-anthesis development of inferior and superior spikelets in japonica/indica hybrid rice. Plant Physiology and Biochemistry 47, 195–204.
| Hormones in the grains and roots in relation to post-anthesis development of inferior and superior spikelets in japonica/indica hybrid rice.Crossref | GoogleScholarGoogle Scholar | 19117763PubMed |
Zhang H, Li HW, Yuan LM, Wang ZQ, Yang JC, Zhang JH (2012) Post-anthesis alternate wetting and moderate soil drying enhances activities of key enzymes in sucrose-to-starch conversion in inferior spikelets of rice. Journal of Experimental Botany 63, 215–227.
| Post-anthesis alternate wetting and moderate soil drying enhances activities of key enzymes in sucrose-to-starch conversion in inferior spikelets of rice.Crossref | GoogleScholarGoogle Scholar | 21926094PubMed |
Zhao D, MacKown CT, Starks PJ, Kindiger BK (2010) Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays. Crop Science 50, 1537–1545.
| Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays.Crossref | GoogleScholarGoogle Scholar |
Zhiguo E, Li T, Zhang H, Liu Z, Deng H, Sharma S, Wei X, Wang L, Niu B, Chen C (2018) A group of nuclear factor Y transcription factors are sub-functionalized during endosperm development in monocots. Journal of Experimental Botany 69, 2495–2510.
| A group of nuclear factor Y transcription factors are sub-functionalized during endosperm development in monocots.Crossref | GoogleScholarGoogle Scholar | 29514259PubMed |
Zhu GH, Ye NH, Yang JC, Peng XX, Zhang JH (2011) Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. Journal of Experimental Botany 62, 3907–3916.
| Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets.Crossref | GoogleScholarGoogle Scholar |