Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Controlling the trade-off between spikelet number and grain filling: the hierarchy of starch synthesis in spikelets of rice panicle in relation to hormone dynamics

Rashmi Panigrahi A * , Ekamber Kariali A * , Binay Bhusan Panda B , Tanguy Lafarge C D and Pravat Kumar Mohapatra https://orcid.org/0000-0002-3519-0911 A E
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Sambalpur University, Jyoti vihar, Sambalpur, 768019, India.

B Environmental Biotechnology Laboratory, Institute of Life Science, Bhubaneswar, 751023, India.

C CIRAD, UMR AGAP, F-34398 Montpellier, France.

D AGAP, University of Montpellier, CIRAD, INRA, INRIA, Montpellier SupAgro, Montpellier, France.

E Corresponding author. Emails: pravat1948@rediffmail.com

Functional Plant Biology 46(6) 507-523 https://doi.org/10.1071/FP18153
Submitted: 12 June 2018  Accepted: 13 February 2019   Published: 9 April 2019

Abstract

The advent of dwarf statured rice varieties enabled a major breakthrough in yield and production, but raising the ceiling of genetically determined yield potential even further has been the breeding priority. Grain filling is asynchronous in the rice panicle; the inferior spikelets particularly on secondary branches of the basal part do not produce grains of a quality suitable for human consumption. Of the various strategies being considered, the control of ethylene production at anthesis has been a valuable route to potentially enhance genetic yield level of rice. The physiology underlying spikelet development has revealed spikelet position-specific ethylene levels determine the extent of grain filling, with higher levels resulting in ill-developed spikelet embodying poor endosperm starch content. To break the yield barrier, breeders have increased spikelet number per panicle in new large-panicle rice plants. However, the advantage of panicles with numerous spikelets has not resulted in enhanced yield because of poor filling of inferior spikelets. High spikelet number stimulates ethylene production and downgrading of starch synthesis, suggesting a trade-off between spikelet number and grain filling. High ethylene production in inferior spikelets suppresses expression of genes encoding endosperm starch synthesising enzymes. Hence, ethylene could be a retrograde signal that dictates the transcriptome dynamics for the cross talk between spikelet number and grain filling in the rice panicle, so attenuation of its activity may provide a solution to the problem of poor grain filling in large-panicle rice. This physiological linkage that reduces starch biosynthesis of inferior kernels is not genetically constitutive and amenable for modification through chemical, biotechnological, surgical and allelic manipulations. Studies on plant genotypes with different panicle architecture have opened up possibilities of selectively improving starch biosynthesis of inferior spikelets and thereby increasing grain yield through a physiological route.

Additional keywords: apical dominance, ethylene, grain filling, starch metabolism, Oryza spp.


References

Adriani DE, Dingkuhn M, Dardou A, Adam H, Luquet D, Lafarge T (2016a) Rice panicle plasticity in near isogenic line carrying a QTL for larger panicle is genotype and environment dependent. Rice 9, 28
Rice panicle plasticity in near isogenic line carrying a QTL for larger panicle is genotype and environment dependent.Crossref | GoogleScholarGoogle Scholar | 27255512PubMed |

Adriani DE, Lafarge T, Dardou A, Fabro A, Clément-Vidal A, Yahya S, Dingkuhn M, Luquet D (2016b) The qTSN positive effect on panicle and flag leaf size of rice is associated with an early down-regulation of tillering. Frontiers in Plant Science 6, 1197
The qTSN positive effect on panicle and flag leaf size of rice is associated with an early down-regulation of tillering.Crossref | GoogleScholarGoogle Scholar | 26779230PubMed |

Afza R, Shen M, Zapata-Arias FJ, Xie J, Fundi HK, Lee K-S, Bobadilla-Mucino E, Kodym A (2000) Effect of spikelet position on rice anther culture efficiency. Plant Science 153, 155–159.
Effect of spikelet position on rice anther culture efficiency.Crossref | GoogleScholarGoogle Scholar | 10717321PubMed |

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 |

Bueno C, Lafarge T (2009) Higher performance of rice hybrids than of elite inbreds in the tropics: 1. Hybrids accumulate more biomass during each phenological phase. Field Crops Research 112, 229–237.
Higher performance of rice hybrids than of elite inbreds in the tropics: 1. Hybrids accumulate more biomass during each phenological phase.Crossref | GoogleScholarGoogle Scholar |

Bueno C, Lafarge T (2017) Maturity groups and growing seasons as key sources of variation to consider within breeding programs for high yielding rice in the tropics. Euphytica 213, 74
Maturity groups and growing seasons as key sources of variation to consider within breeding programs for high yielding rice in the tropics.Crossref | GoogleScholarGoogle Scholar |

Bueno C, Pasuquin E, Tubaña B, Lafarge T (2010) Improving sink regulation, and searching for promising traits associated with hybrids, as a key avenue to increase yield potential of the rice crop in the tropics. Field Crops Research 118, 199–207.
Improving sink regulation, and searching for promising traits associated with hybrids, as a key avenue to increase yield potential of the rice crop in the tropics.Crossref | GoogleScholarGoogle Scholar |

Choi S-B, Zhang Y, Ito H, Stephens K, Winder T, Edwards GE, Okita TW (1998) Increasing rice productivity by manipulation of starch biosynthesis during seed development. In ‘Feeding a world population of more than eight billion people: a challenge to science’. (Eds JC Waterlow, DG Armstrong, L Fowden, R Riley) pp. 137–149. (Oxford University Press: New York)

Counce PA, Gravois KA (2006) Sucrose synthase activity as a potential indicator of high rice grain yield. Crop Science 46, 1501–1507.
Sucrose synthase activity as a potential indicator of high rice grain yield.Crossref | GoogleScholarGoogle Scholar |

Dante RA, Sabelli PA, Nguyen HN, Leivo-Neto JT, Tao Y, Lowe KS, Hoerster GJ, Gordon-Kamm WJ, Jung R, Larkins BA (2014) Cyclin-dependent kinase complexes in developing maize endosperm: evidence for differential expression and functional specialization. Planta 239, 493–509.
Cyclin-dependent kinase complexes in developing maize endosperm: evidence for differential expression and functional specialization.Crossref | GoogleScholarGoogle Scholar | 24240479PubMed |

Das K, Panda BB, Shaw BP, Das SR, Dash SK, Kariali E, Mohapatra PK (2018) Grain density and its impact on grain filling characteristic of rice: mechanistic testing of the concept in genetically related cultivars. Scientific Reports 8, 4149
Grain density and its impact on grain filling characteristic of rice: mechanistic testing of the concept in genetically related cultivars.Crossref | GoogleScholarGoogle Scholar | 29515145PubMed |

Fabre D, Adriani DE, Dingkuhn M, Ishimaru T, Punzalan B, Lafarge T, Clement-Vidal A, Luquet D (2016) The qTSN4 effect on flag leaf size, photosynthesis and panicle size, benefits to plant grain production in rice depending on light availability. Frontiers in Plant Science 7, 623
The qTSN4 effect on flag leaf size, photosynthesis and panicle size, benefits to plant grain production in rice depending on light availability.Crossref | GoogleScholarGoogle Scholar | 27242827PubMed |

Fitzgerald MA, Mccouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends in Plant Science 14, 133–139.
Not just a grain of rice: the quest for quality.Crossref | GoogleScholarGoogle Scholar | 19230745PubMed |

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 |

Furbank RT, Scoefield GN, Hirose T, Wang X-D, Patrick JW, Offler CE (2001) Cellular localisation and function of a sucrose transporter OsSUT1 in developing rice grains. Australian Journal of Plant Physiology 28, 1187–1196.

GRiSP (2013) ‘Rice almanc.’ (4th edn) (International Rice Research Institute: Los Banos, Philippines)

Hirose T, Terao T (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220, 9–16.
A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 15232694PubMed |

Hirose T, Takano M, Terao T (2002) Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant & Cell Physiology 43, 452–459.
Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling.Crossref | GoogleScholarGoogle Scholar |

Hirose T, Scoefield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Science 174, 534–543.
An expression analysis profile for the entire sucrose synthase gene family in rice.Crossref | GoogleScholarGoogle Scholar |

Hoshikawa K (1993) Anthesis, fertilization and development of caryopsis. In ‘Science of rice plant. Vol. I Morphology’. (Eds T Matsuo, K Hoshikawa) pp. 339–376. (Food and Agricultural Policy Research Center Tokyo, Japan)

Hwang JW, Kim SK, Lee JS, Kim IS (2005) Gene Expression of the biosynthetic enzymes and biosynthesis of starch during rice grain development. Journal of Plant Biology 48, 448–455.
Gene Expression of the biosynthetic enzymes and biosynthesis of starch during rice grain development.Crossref | GoogleScholarGoogle Scholar |

Hwang SK, Singh S, Cakir B, Satoh H, Okita TW (2016a) The plastidial starch phosphorylase from rice endosperm: catalytic properties at low temperature. Planta 243, 999–1009.
The plastidial starch phosphorylase from rice endosperm: catalytic properties at low temperature.Crossref | GoogleScholarGoogle Scholar | 26748915PubMed |

Hwang SK, Koper K, Satoh H, Okita TW (2016b) Rice endosperm starch phosphorylase (Pho1) assembles with disproportionating enzyme (Dpe1) to form a protein complex that enhances synthesis of malto-oligosaccharides. Journal of Biological Chemistry 291, 19994–20007.
Rice endosperm starch phosphorylase (Pho1) assembles with disproportionating enzyme (Dpe1) to form a protein complex that enhances synthesis of malto-oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 27502283PubMed |

Ishimaru T, Matsuda T, Ohsugi R, Yamagishi T (2003) Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling. Functional Plant Biology 30, 1139–1149.
Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling.Crossref | GoogleScholarGoogle Scholar |

Ishimaru T, Hirose T, Matsuda T, Goto A, Takahashi K, Sasaki H, Terao T, Ishii R, Ohsugi R, Yamagishi T (2005) Expression patterns of genes encoding carbohydrate-metabolizing enzymes and their relationship to grain filling in rice (Oryza sativa L.): comparison of caryopses located at different positions in a panicle. Plant & Cell Physiology 46, 620–628.
Expression patterns of genes encoding carbohydrate-metabolizing enzymes and their relationship to grain filling in rice (Oryza sativa L.): comparison of caryopses located at different positions in a panicle.Crossref | GoogleScholarGoogle Scholar |

Jeng TL, Wang CS, Chen CL, Sung JM (2003) Effects of grain position on the panicle on starch biosynthetic enzyme activity in developing grains of rice cultivar Tainung 67 and its NaN3-induced mutant. Journal of Agricultural Science 141, 303–311.
Effects of grain position on the panicle on starch biosynthetic enzyme activity in developing grains of rice cultivar Tainung 67 and its NaN3-induced mutant.Crossref | GoogleScholarGoogle Scholar |

Jeon J-S, Ryoo N, Hahn T-R, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry 48, 383–392.
Starch biosynthesis in cereal endosperm.Crossref | GoogleScholarGoogle Scholar | 20400324PubMed |

Kato T (1995) Change of sucrose synthase activity in developing endosperm of rice cultivars. Crop Science 35, 827–831.
Change of sucrose synthase activity in developing endosperm of rice cultivars.Crossref | GoogleScholarGoogle Scholar |

Kato T (2004) Effect of spikelet removal on grain filling of Akenohoshi, a rice cultivar with numerous spikelets in a panicle. Journal of Agricultural Sciences 142, 177–181.

Kato T, Takeda K (1993) Endogenous abscisic acid in developing grains on primary and secondary branches of rice (Oryza sativa L.). Nihon Sakumotsu Gakkai Kiji 62, 636–637.
Endogenous abscisic acid in developing grains on primary and secondary branches of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Kato T, Sakurai N, Kuraishi N (1993) The changes of endogenous abscisic acid in developing grains of two rice cultivars with different grain size. Nihon Sakumotsu Gakkai Kiji 62, 456–461.
The changes of endogenous abscisic acid in developing grains of two rice cultivars with different grain size.Crossref | GoogleScholarGoogle Scholar |

Kato T, Shinmura D, Taniguchi A (2007) Activities of enzymes for sucrose–starch conversion in developing endosperm of rice and their association with grain filling in extra-heavy panicle types. Plant Production Science 10, 442–450.
Activities of enzymes for sucrose–starch conversion in developing endosperm of rice and their association with grain filling in extra-heavy panicle types.Crossref | GoogleScholarGoogle Scholar |

Kato T, Taniguchi A, Horibata A (2010) Effects of the alleles at OsAPGS2 and OsSUT1 on the grain filling of extra heavy panicle type of rice. Crop Science 50, 2448–2456.
Effects of the alleles at OsAPGS2 and OsSUT1 on the grain filling of extra heavy panicle type of rice.Crossref | GoogleScholarGoogle Scholar |

Khush GS (2013) Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breeding 132, 433–436.

Khush GS, Peng S (1996) Breaking the yield frontier of rice. In ‘Increasing yield potential in wheat: breaking the barriers. Proceedings of a workshop held on 26–28 March 1996 in Ciudad Obregon, Sonora, Mexico’. pp. 36–49. (International Maize and Wheat Improvement Center: Mexico)

Kosar-Hashemi B, Li Z, Larroque O, Regina A, Yamamori M, Morell MK, Rahman S (2007) Multiple effects of starch synthase II mutation in developing wheat endosperm. Functional Plant Biology 34, 431–438.
Multiple effects of starch synthase II mutation in developing wheat endosperm.Crossref | GoogleScholarGoogle Scholar |

Kuanar S, Panigrahi R, Kariali E, Mohapatra PK (2010) Apoplasmic assimilates and grain growth of contrasting rice cultivars differing in grain dry mass and size. Plant Growth Regulation 61, 135–151.
Apoplasmic assimilates and grain growth of contrasting rice cultivars differing in grain dry mass and size.Crossref | GoogleScholarGoogle Scholar |

Lafarge T, Bueno C (2009) Higher performance of rice hybrids than of elite inbreds in the tropics: 2. Does sink regulation, rather than sink size, play a major role? Field Crops Research 114, 434–440.
Higher performance of rice hybrids than of elite inbreds in the tropics: 2. Does sink regulation, rather than sink size, play a major role?Crossref | GoogleScholarGoogle Scholar |

Li B, Liu H, Zhang Y, Kang T, Zhang L, Tong J, Xiao L, Zhang H (2013) Constitutive expression of cell wall invertase genes increases grain yield and starch content in maize. Plant Biotechnology Journal 11, 1080–1091.
Constitutive expression of cell wall invertase genes increases grain yield and starch content in maize.Crossref | GoogleScholarGoogle Scholar | 23926950PubMed |

Li G, Pan J, Cui K, Yuan M, Hu Q, Wang W, Mohapatra PK, Nie L, Huang J, Peng S (2017) Limitation of unloading in the developing grains is a possible cause responsible for low stem non-structural carbohydrate translocation and poor grain yield formation in rice through verification of recombinant inbred lines. Frontiers in Plant Science 8, 1369
Limitation of unloading in the developing grains is a possible cause responsible for low stem non-structural carbohydrate translocation and poor grain yield formation in rice through verification of recombinant inbred lines.Crossref | GoogleScholarGoogle Scholar | 28848573PubMed |

Liang J, Zhang J, Cao X (2001) Grain sink strength may be related to the poor grain filling of indica-japonica rice (Oryza sativa L.) hybrids. Physiologia Plantarum 112, 470–477.
Grain sink strength may be related to the poor grain filling of indica-japonica rice (Oryza sativa L.) hybrids.Crossref | GoogleScholarGoogle Scholar | 11473706PubMed |

Liu K, Ye Y, Tang C, Wang Z, Yang J (2008) Response of ethylene and ACC in rice grains to soil moisture and their relation to grain filling. Frontiers of Agriculture in China 2, 172–180.
Response of ethylene and ACC in rice grains to soil moisture and their relation to grain filling.Crossref | GoogleScholarGoogle Scholar |

Lu FH, Park YJ (2012) Sequence variations in OsAGPase significantly associated with amylose content and viscosity properties in rice (Oryza sativa L.). Genetical Research 94, 179–189.
Sequence variations in OsAGPase significantly associated with amylose content and viscosity properties in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Mizutani M, Naganuma T, Tsutsumi K, Saitoh Y (2010) The syncytium-specific expression of the Orysa;KRP3 CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm. Journal of Experimental Botany 61, 791–798.
The syncytium-specific expression of the Orysa;KRP3 CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm.Crossref | GoogleScholarGoogle Scholar | 19933315PubMed |

Mohapatra PK (2012) Sucrose metabolism and grain development of contrasting spikelets located at different positions of the rice panicle. In ‘Progress in food science and technology. Vol.1’. (Ed. AJ Greco) pp. 231–241. (Nova Science Publishers: Hauppauge, NY, USA)

Mohapatra PK (2013) A physiological approach to design rice panicle architecture in the quest for high grain yield. In ‘International dialogue on perception and prospects of designer rice’. (Eds K Muralidharan, EA Siddiq) pp. 131–142. (Society for Advancement of Rice Research, Directorate of Rice Research: Hyderabad, India)

Mohapatra R, Mohapatra PK (2006) Ethylene control of seed coat development in low and high sterile semi-dwarf indica rice cultivars. Plant Growth Regulation 50, 47–55.
Ethylene control of seed coat development in low and high sterile semi-dwarf indica rice cultivars.Crossref | GoogleScholarGoogle Scholar |

Mohapatra PK, Sahu SK (1991) Heterogeneity of primary branch development and spikelet survival in rice in relation to assimilate contents of primary branches. Journal of Experimental Botany 42, 871–879.
Heterogeneity of primary branch development and spikelet survival in rice in relation to assimilate contents of primary branches.Crossref | GoogleScholarGoogle Scholar |

Mohapatra PK, Patel R, Sahu SK (1993) Time of flowering affects grain quality and spikelet partitioning within rice panicle. Australian Journal of Plant Physiology 20, 231–241.

Mohapatra PK, Naik PK, Patel R (2000) Ethylene inhibitors improve dry matter partitioning and development of late flowering spikelets on rice panicles. Australian Journal of Plant Physiology 27, 311–323.

Mohapatra PK, Masamoto Y, Morita S, Takanashi J, Kato T, Itani T, Adu-Gyamfi JJ, Shunmugasundaram M, Nguyen NT, Saneoka H, Fujita K (2004) Partitioning of 13C-labelled photosynthate varies with growth stage and paniclesize in high yielding rice. Functional Plant Biology 31, 131–139.
Partitioning of 13C-labelled photosynthate varies with growth stage and paniclesize in high yielding rice.Crossref | GoogleScholarGoogle Scholar |

Mohapatra PK, Sarkar RK, Kuanar SR (2009) Starch synthesizing enzymes and sink strength of grains of contrasting rice cultivars. Plant Science 176, 256–263.
Starch synthesizing enzymes and sink strength of grains of contrasting rice cultivars.Crossref | GoogleScholarGoogle Scholar |

Mohapatra PK, Panigrahi R, Turner NC (2011) Physiology of spikelet development in rice: is manipulation of apical dominance crucial for grain yield. Advances in Agronomy 110, 333–359.
Physiology of spikelet development in rice: is manipulation of apical dominance crucial for grain yield.Crossref | GoogleScholarGoogle Scholar |

Morey SR, Hirose T, Hashida Y, Miyao A, Hirochika H, Ohsugi R, Yamagishi J, Aoki N (2018) Genetic evidence for the role of a rice vacuolar invertase as a molecular sink strength determinant. Rice 11, 6
Genetic evidence for the role of a rice vacuolar invertase as a molecular sink strength determinant.Crossref | GoogleScholarGoogle Scholar | 29344835PubMed |

Morgan PW, Finlayson SA, Childs KL, Mullet JE, Rooney WL (2002) Opportunities to improve adaptability and grain yield in grasses. Lessons from sorghum. Crop Science 42, 1791–1799.
Opportunities to improve adaptability and grain yield in grasses. Lessons from sorghum.Crossref | GoogleScholarGoogle Scholar |

Müller D, Leyser O (2011) Auxin, cytokinin and the control of shoot branching. Annals of Botany 107, 1203–1212.
Auxin, cytokinin and the control of shoot branching.Crossref | GoogleScholarGoogle Scholar | 21504914PubMed |

Naik PK, Mohapatra PK (2000) Ethylene inhibitors enhanced sucrose synthase activity and promoted grain filling of basal rice kernels. Australian Journal of Plant Physiology 27, 997–1008.

Nakamura Y, Yuki K, Park SY (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant & Cell Physiology 30, 833–839.
Carbohydrate metabolism in the developing endosperm of rice grains.Crossref | GoogleScholarGoogle Scholar |

Nakamura Y, Ono M, Sawada T, Crofts N, Fujita N, Steup M (2017) Characterization of the functional interactions of plastidial starch phosphorylase and starch branching enzymes from rice endosperm during reserve starch biosynthesis. Plant Science 264, 83–95.
Characterization of the functional interactions of plastidial starch phosphorylase and starch branching enzymes from rice endosperm during reserve starch biosynthesis.Crossref | GoogleScholarGoogle Scholar | 28969805PubMed |

Neelam K, Kumar K, Dhaliwal HS, Singh K (2016) Introgression and exploitation of QTL for yield and yield components from related wild species in rice cultivars. In ‘Molecular breeding for sustainable crop improvement, sustainable development and biodiversity’. (Eds VR Rajpal, SR Rao, SN Raina) pp. 171–202. (Springer International Publishing: AG, Switzerland)

Ohdan T, Franscico 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 | 16275672PubMed |

Panda BB, Kariali E, Panigarhi R, Mohapatra PK (2009) High ethylene production slackens grain filling in compact panicle rice cultivar. Plant Growth Regulation 58, 141–151.
High ethylene production slackens grain filling in compact panicle rice cultivar.Crossref | GoogleScholarGoogle Scholar |

Panda BB, Badoghar A, Das K, Panigrahi R, Kariali E, Das SR, Dash SK, Shaw BP, Mohapatra PK (2015) Compact panicle architecture is detrimental for growth as well as sucrose synthase activity of developing rice kernels. Functional Plant Biology 42, 875–887.
Compact panicle architecture is detrimental for growth as well as sucrose synthase activity of developing rice kernels.Crossref | GoogleScholarGoogle Scholar |

Panda BB, Badoghar A, Sekhar S, Shaw BP, Mohapatra PK (2016) 1-MCP treatment enhanced expression of genes controlling endosperm cell division and starch biosynthesis for improvement of grain filling in a dense-panicle rice cultivar. Plant Science 246, 11–25.
1-MCP treatment enhanced expression of genes controlling endosperm cell division and starch biosynthesis for improvement of grain filling in a dense-panicle rice cultivar.Crossref | GoogleScholarGoogle Scholar | 26993232PubMed |

Patel R, Mohapatra PK (1992) Regulation of spikelet development in rice by hormones. Journal of Experimental Botany 43, 257–262.
Regulation of spikelet development in rice by hormones.Crossref | GoogleScholarGoogle Scholar |

Patel R, Mohapatra PK (1996) Assimilate partitioning within floret components of contrasting rice spikelets producing qualitatively different types of grains. Australian Journal of Plant Physiology 23, 85–92.

Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS (1999) Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Science 39, 1552–1559.
Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential.Crossref | GoogleScholarGoogle Scholar |

Peng S, Khush GS, Virk P, Tang Q, Zou Q (2008) Progress in ideotype breeding to increase rice yield potential. Field Crops Research 108, 32–38.
Progress in ideotype breeding to increase rice yield potential.Crossref | GoogleScholarGoogle Scholar |

Sekhar S, Panda BB, Mohapatra T, Das K, Shaw BP, Kariali E, Mohapatra PK (2015) Spikelet-specific variation in ethylene production and constitutive expression of ethylene receptors and signal transducers during grain filling of compact- and lax-panicle rice (Oryza sativa L.) cultivars Journal of Plant Physiology 179, 21–34.
Spikelet-specific variation in ethylene production and constitutive expression of ethylene receptors and signal transducers during grain filling of compact- and lax-panicle rice (Oryza sativa L.) cultivarsCrossref | GoogleScholarGoogle Scholar | 25817414PubMed |

Setter TL, Conocono EA, Egdane JA (1996) Possibility of increasing yield potential of rice by reducing panicle height in the canopy. II. Canopy photosynthesis and yield of isogenic lines. Australian Journal of Plant Physiology 23, 161–169.

Smidansky ED, Martin JM, Hannah LC, Fischer AM, Giroux MJ (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216, 656–664.

Sun L, Yang D-L, Kong Y, Chen Y, Li X-Z, Zeng L-J, Li Q, Wang E-T, He Z-H (2014) Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defense in rice. Molecular Plant Pathology 15, 161–173.
Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defense in rice.Crossref | GoogleScholarGoogle Scholar | 24118770PubMed |

Taiz L, Zeiger E (2002) Translocation in the phloem. In ‘Plant physiology’. (3rd edn) , pp. 193–221. (Sinauer Associates, Inc.: Sunderland, MA, USA)

Takaiwa F, Qu L (2010) AGPase promoter from rice and its uses thereof. United States Patent No.7700835 B2 dated 20 April 2010.

Umemoto T, Terashima K (2002) Activity of granule bound starch synthase is an important determinant of amylase content in rice endosperm. Functional Plant Biology 29, 1121–1124.
Activity of granule bound starch synthase is an important determinant of amylase content in rice endosperm.Crossref | GoogleScholarGoogle Scholar |

Umemoto T, Nakamura Y, Ishikura N (1994) Effect of grain location on the panicle on activities involved in starch synthesis in rice endosperm. Phytochemistry 36, 843–847.
Effect of grain location on the panicle on activities involved in starch synthesis in rice endosperm.Crossref | GoogleScholarGoogle Scholar |

Valluru R, Reynolds MP, Davis WJ, Sukumaran S (2016) Phenotypic and genome-wide association analysis of spike ethylene in diverse wheat genotypes under heat stress. New Phytologist
Phenotypic and genome-wide association analysis of spike ethylene in diverse wheat genotypes under heat stress.Crossref | GoogleScholarGoogle Scholar | 27918628PubMed |

Vandeputte GE, Delcour JA (2004) From sucrose to starch granule to starch physical behavior: a focus on rice starch. Carbohydrate Polymers 58, 245–266.
From sucrose to starch granule to starch physical behavior: a focus on rice starch.Crossref | GoogleScholarGoogle Scholar |

Virmani SS, Aquino RC, Khush GS (1982) Heterosis breeding in rice (Oryza sativa L.). Theoretical and Applied Genetics 63, 373–380.
Heterosis breeding in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 24270875PubMed |

Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z (2008) Control of rice grain-filling and yield by a gene with potential signature of domestication. Nature Genetics 40, 1370–1374.
Control of rice grain-filling and yield by a gene with potential signature of domestication.Crossref | GoogleScholarGoogle Scholar | 18820698PubMed |

Wang E, Xu X, Zhang L, Zhang H, Lin L, Wang Q, Li Q, Ge S, Lu BR, Wang W, He Z (2010a) Duplication and independent selection of cell wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication. BMC Evolutionary Biology 10, 108–121.
Duplication and independent selection of cell wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication.Crossref | GoogleScholarGoogle Scholar | 20416079PubMed |

Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010b) A dynamic gene expression atlas covering the entire life cycle of rice. The Plant Journal 61, 752–766.
A dynamic gene expression atlas covering the entire life cycle of rice.Crossref | GoogleScholarGoogle Scholar | 20003165PubMed |

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 |

Xing Y, Zhang Q (2010) Genetics and molecular bases of rice yield. Annual Review of Plant Biology 61, 421–442.
Genetics and molecular bases of rice yield.Crossref | GoogleScholarGoogle Scholar | 20192739PubMed |

Xu X, Vergara BS (1986) Morphological changes in rice panicle development. A review of literature. IRRI Research Paper Series No. 117. International Rice Research Institute, Manila, The Philippines.

Xu ZJ, Chen WF, Zhang LB, Yang SR (1990) Comparative study on light distribution in rice canopies with different panicle types. Zhongguo Nong Ye Ke Xue 23, 6–10.

Yamagishi T, Peng S, Cassman KG, Ishii R (1996) Studies on grain filling characteristics in ‘New Plant Type’ rice lines developed in IRRI. Japanese Journal of Crop Science 65, 169–170.

Yamagishi M, Takeuchi Y, Kono I, Yano M (2002) QTL analysis for panicle characteristics in temperate japonica rice. Euphytica 128, 219–224.
QTL analysis for panicle characteristics in temperate japonica rice.Crossref | GoogleScholarGoogle Scholar |

Yang J, Zhang J (2010) Grain filling problems in ‘super’ rice. Journal of Experimental Botany 61, 1–5.
Grain filling problems in ‘super’ rice.Crossref | GoogleScholarGoogle Scholar | 19959608PubMed |

Yang J, Peng S, Gu S, Visperas RM, Zhu Q (2000) Grain filling pattern and cytokinin content in the grains and roots of rice plants. Plant Growth Regulation 30, 261–270.
Grain filling pattern and cytokinin content in the grains and roots of rice plants.Crossref | GoogleScholarGoogle Scholar |

Yang J, Peng S, Zhang J, Wang Z, Visperas RM, Zhu Q (2002) Grain and dry matter yields and partitioning of assimilates in japonica/indica hybrid rice. Crop Science 42, 766–772.
Grain and dry matter yields and partitioning of assimilates in japonica/indica hybrid rice.Crossref | GoogleScholarGoogle Scholar |

Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2003) Activities of enzymes involved in sucrose to starch metabolism in rice grains subjected to water stress during filling. Field Crops Research 81, 69–81.
Activities of enzymes involved in sucrose to starch metabolism in rice grains subjected to water stress during filling.Crossref | GoogleScholarGoogle Scholar |

Yang J, Zhang J, Wang Z, Liu K, Wang P (2006) Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. Journal of Experimental Botany 57, 149–160.
Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene.Crossref | GoogleScholarGoogle Scholar | 16330527PubMed |

Yang W, Peng S, Laza RC, Visperas RM, Dionisio-Sese ML (2007) Grain yield and yield attributes of new plant type and hybrid rice. Crop Science 47, 1393–1400.
Grain yield and yield attributes of new plant type and hybrid rice.Crossref | GoogleScholarGoogle Scholar |

Yin C-C, Zhao H, Ma B, Chen S-Y, Zhang J-S (2017) Diverse roles of ethylene in regulating agronomic traits in rice. Frontiers in Plant Science 8, 1676
Diverse roles of ethylene in regulating agronomic traits in rice.Crossref | GoogleScholarGoogle Scholar | 29018471PubMed |

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

You C, Zhu H, Xu B, Huang W, Wang S, Ding Y, Liu Z, Li G, Chen L, Ding C, Tang S (2016) Effect of removing superior spikelets on grain filling of inferior spikelets in rice. Frontiers in Plant Science 7, 1161
Effect of removing superior spikelets on grain filling of inferior spikelets in rice.Crossref | GoogleScholarGoogle Scholar | 27547210PubMed |

Zhang H, Tan G, Yang L, Yang J, Zhang J, Zhao B (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 Z, Zhao H, Tang J, Li Z, Li Z, Chen D, Lin X (2014) A proteomic study on molecular mechanism of poor grain filling of rice (Oryza sativa L.) inferior spikelets. PLoS ONE 9, e89140
A proteomic study on molecular mechanism of poor grain filling of rice (Oryza sativa L.) inferior spikelets.Crossref | GoogleScholarGoogle Scholar | 25549324PubMed |

Zhang W, Cao Z, Zhou Q, Chen J, Xu G, Gu J, Liu L, Wang Z, Yang J, Zhang H (2016) Grain filling characteristics and their relations with endogenous hormones in large- and small-grain mutants of rice. PLoS One 11, e0165321
Grain filling characteristics and their relations with endogenous hormones in large- and small-grain mutants of rice.Crossref | GoogleScholarGoogle Scholar | 28033377PubMed |

Zhu G, Ye N, Yang J, Peng X, Zhang J (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 | 21459770PubMed |