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

Cell cycle events and expression of cell cycle regulators are determining factors in differential grain filling in rice spikelets based on their spatial location on compact panicles

Gyanasri Sahu A , Binay B. Panda A , Sushanta K. Dash B , Tilak Chandra A and Birendra P. Shaw https://orcid.org/0000-0003-0541-3296 A C
+ Author Affiliations
- Author Affiliations

A Abiotic Stress and Agro-Biotechnology Laboratory, Institute of Life Sciences, Nalco Square, Bhubaneswar 751023, Odisha, India.

B Crop Improvement Division, ICAR-National Rice Research Institute (Formerly Central Rice Research Institute), Cuttack, Odisha, India.

C Corresponding author. Email: b_p_shaw@yahoo.com

Functional Plant Biology - https://doi.org/10.1071/FP20196
Submitted: 6 July 2020  Accepted: 23 September 2020   Published online: 30 October 2020

Abstract

Rice being a staple crop for human, its production is required to be increased significantly, particularly keeping in view the expected world’s population of 9.6 billion by the year 2050. In this context, although the rice breeding programs have been successful in increasing the number of spikelets per panicle, the basal spikelets remain poorly filled, undermining the yield potential. The present study also found the grain filling to bear negative correlation with the panicle grain density. The poorly filled basal spikelets of the compact-panicle cultivars showed a lower endosperm cell division rate and ploidy status of the endosperm nuclei coupled with no significant greater expression of CYCB;1 and CYCH;1 compared with the apical spikelets, unlike that observed in the lax-panicle cultivars, which might have prevented them from overcoming apical dominance. Significantly greater expression of CYCB2;2 in the basal spikelets than in the apical spikelets might also have prevented the former to enter into endoreduplication. Furthermore, expression studies of KRPs in the caryopses revealed that a higher expression of KRP;1 and KRP;4 in the basal spikelets than in the apical spikelets of the compact-panicle cultivars could also be detrimental to grain filling in the former, as KRPs form complex primarily with CDKA-CYCD that promotes S-phase activity and G1/S transition, and thus inhibits endosperm cell division. The study indicates that targeted manipulation of expression of CYCB1;1, CYCB2;2, CYCH1;1, KRP;1 and KRP4 in the basal spikelets of the compact-panicle cultivars may significantly improve their yield performance.

Keywords: CDKs, cyclins, endosperm, KRPs, Oryza sativa, panicle morphology, rice, yield.


References

Ajadi AA, Xiaohong Tong X, Wang H, Juan Zhao J, Tang L, Li Z, Liu X, Yazhou Shu Y, Li S, Wang S, Wanning Liu W, Tajo SM, Zhang J, Wan Y (2020) Cyclin-dependent kinase inhibitors KRP1 and KRP2 are involved in grain filling and seed germination in rice (Oryza sativa L.). International Journal of Molecular Sciences 21, 245
Cyclin-dependent kinase inhibitors KRP1 and KRP2 are involved in grain filling and seed germination in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Barrôco RM, Peres A, Droual A-M, De Veylder L, Nguyen LSL, Wolf JD, Mironov V, Peerbolte R, Beemster GTS, Inze D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in seed development of rice. Plant Physiology 142, 1053–1064.
The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in seed development of rice.Crossref | GoogleScholarGoogle Scholar | 17012406PubMed |

Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, Hilson P, Inze D, De Velder L, Russinova E (2010) Functional modules in the Arabidopsis core cell cycle binary protein–protein interaction network. The Plant Cell 22, 1264–1280.
Functional modules in the Arabidopsis core cell cycle binary protein–protein interaction network.Crossref | GoogleScholarGoogle Scholar | 20407024PubMed |

Brown SC, Bergounioux C, Tallet S, Marie D (1991) Flow cytometry of nuclei for ploidy and cell cycle analysis, In ‘A laboratory guide for cellular and molecular plant biology’. (Eds I Negrutiu, G Gharti-Chhetr) pp 326–345. (Birkhäuser: Basel)

Cheng S-H, Cao L-Y, Zhuang J-Y, Chen S-G, Zhan X-D, Fan Y-Y, Zhu D-F, Min S-K (2007) Super hybrid rice breeding in China: achievements and prospects. Journal of Integrative Plant Biology 49, 805–810.
Super hybrid rice breeding in China: achievements and prospects.Crossref | GoogleScholarGoogle Scholar |

Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin J-P, Gevaudant F, Hernould M (2011) Elucidating the functional role of endoreduplication in tomato fruit development. Annals of Botany 107, 1159–1169.
Elucidating the functional role of endoreduplication in tomato fruit development.Crossref | GoogleScholarGoogle Scholar | 21199834PubMed |

Cockcroft CE, den Boer BGW, Healy JMS, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405, 575–579.
Cyclin D control of growth rate in plants.Crossref | GoogleScholarGoogle Scholar | 10850717PubMed |

D’Amato F (1984) Role of polyploidy in reproductive organs and tissues. In ‘Embryology of angiosperms’. (Ed. BM Johri) pp. 523–566. (Springer-Verlag: New York)

Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Frontiers in Plant Science 5, 493
Cell cycle control and seed development.Crossref | GoogleScholarGoogle Scholar | 25295050PubMed |

De Veylder L, Beeckman T, Beemster GTS, Krols L, Terras F, Landrieu I, Schueren EVD, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. The Plant Cell 13, 1653–1667.
Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11449057PubMed |

Doerner P, Jorgensen JE, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380, 520–523.
Control of root growth and development by cyclin expression.Crossref | GoogleScholarGoogle Scholar | 8606769PubMed |

Dudits D, Cserháti M, Miskolczi P, Horváth GV (2007) The growing family of plant cyclin-dependent kinases with multiple functions in cellular and developmental regulation. In ‘Cell cycle control and plant development. Annual Plant Reviews, Vol. 32’. (Ed. D Inze) pp. 1–30. (Blackwell Publishing Ltd: Oxford)

FAO (2018) Rice market monitor. Available at http://www.fao.org/3/I9243EN/i9243en.pdf [Verified 28 September 2020]

FAO (2019) World food situation. Available at http://www.fao.org/worldfoodsituation/csdb/en/ [Verified 28 September 2020]

Guo J, Song J, Wang F, Zhang XS (2007) Genome-wide identification and expression analysis of rice cell cycle genes Plant Molecular Biology 64, 349–360.
Genome-wide identification and expression analysis of rice cell cycle genesCrossref | GoogleScholarGoogle Scholar | 17443292PubMed |

Guo J, Wang F, Song J, Sun W, Zhang XS (2010) The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta 231, 293–303.
The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice.Crossref | GoogleScholarGoogle Scholar | 19921249PubMed |

Inukai T (2017) Differential regulation of starch-synthetic gene expression in endosperm between Indica and Japonica rice cultivars. Rice 10, 7
Differential regulation of starch-synthetic gene expression in endosperm between Indica and Japonica rice cultivars.Crossref | GoogleScholarGoogle Scholar | 28243987PubMed |

Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annual Review of Genetics 40, 77–105.
Cell cycle regulation in plant development.Crossref | GoogleScholarGoogle Scholar | 17094738PubMed |

Ishimaru T, Hirose T, Matsuda T, Goto A, Takahashi K, Sasaki H, Terao T, Ishii R-I, 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 |

James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Current Opinion in Plant Biology 6, 215–222.
Starch synthesis in the cereal endosperm.Crossref | GoogleScholarGoogle Scholar | 12753970PubMed |

Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3; 1-overexpressing plants. Journal of Cell Science 115, 973–982.

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

Kitsios G, Doonan JH (2011) Cyclin dependent protein kinases and stress responses in plants. Plant Signaling & Behavior 6, 204–209.
Cyclin dependent protein kinases and stress responses in plants.Crossref | GoogleScholarGoogle Scholar |

Kobayashi H (2019) Variations of endoreduplication and its potential contribution to endosperm development in rice (Oryza sativa L.). Plant Production Science 22, 227–241.
Variations of endoreduplication and its potential contribution to endosperm development in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Kowles RV, Phillips RL (1988) Endosperm development in maize. International Review of Cytology 112, 97–136.
Endosperm development in maize.Crossref | GoogleScholarGoogle Scholar |

Kowles RV, Srienc F, Phillips RL (1990) Endoreduplication of nuclear DNA in the developing maize endosperm. Developmental Genetics 11, 125–132.
Endoreduplication of nuclear DNA in the developing maize endosperm.Crossref | GoogleScholarGoogle Scholar |

La H, Li J, Ji Z, Cheng Y, Li X, Jiang S, Venkatesh PN, Ramchandran S (2006) Genome-wide analysis of cyclin family in rice (Oryza sativa L.). Molecular Genetics and Genomics 275, 374–386.
Genome-wide analysis of cyclin family in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 16435118PubMed |

Lee J, Das A, Yamaguchi M, Hashimoto J, Tsutsumi N, Uchimiya H, Umeda M (2003) Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. The Plant Journal 34, 417–425.
Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase.Crossref | GoogleScholarGoogle Scholar | 12753582PubMed |

Ma YZ, MacKown CT, Sanford DA (1990) Sink manipulation in wheat: compensatory changes in kernel size. Crop Science 30, 1099–1105.
Sink manipulation in wheat: compensatory changes in kernel size.Crossref | GoogleScholarGoogle Scholar |

McKevith B (2004) Nutritional aspects of cereals. Nutrition Bulletin 29, 111–142.
Nutritional aspects of cereals.Crossref | GoogleScholarGoogle Scholar |

Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Current Opinion in Plant Biology 4, 533–539.
A matter of size: developmental control of organ size in plants.Crossref | GoogleScholarGoogle Scholar | 11641070PubMed |

Mizutani M, Naganuma T, Tsutsumi K, Saitoh Y (2010) The syncytium-specific expression of Orysa; KRP3CDK 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 Orysa; KRP3CDK inhibitor: implication of its involvement in the cell cycle control in the rice (Oryza sativa L.) syncytial endosperm.Crossref | GoogleScholarGoogle Scholar | 19933315PubMed |

OECD/FAO (2019) OECD-AFO agricultural outlook 2019–2028. Available at https://www.oecd-ilibrary.org/docserver/agr_outlook-2019-en.pdf?expires=1570019648&id=id&accname=guest&checksum=730BBF630F3B2289BB3D8FC41924655D [Verified 28 September 2020]

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 | 16275672PubMed |

Okamura M, Arai-Sanoha Y, Yoshidab H, Mukouyama T, Adachi S, Yabe S, Nakagawa H, Tsutsumi K, Taniguchi Y, Kobayashi N, Kondo M (2018) Characterization of high-yielding rice cultivars with different grain-filling properties to clarify limiting factors for improving grain yield. Field Crops Research 219, 139–147.
Characterization of high-yielding rice cultivars with different grain-filling properties to clarify limiting factors for improving grain yield.Crossref | GoogleScholarGoogle Scholar |

Olsen OA, Linnestad C, Nichols SE (1999) Developmental biology of the cereal endosperm. Trends in Plant Science 4, 253–257.
Developmental biology of the cereal endosperm.Crossref | GoogleScholarGoogle Scholar | 10407440PubMed |

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

Panda BB, Badoghar AK, 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 | 32480730PubMed |

Panda BB, Badoghar AK, Sekhar S, Shaw BP, Mohapatra PK (2016a) 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 |

Panda BB, Badoghar AK, Sekhar S, Kariali E, Mohapatra PK, Shaw BP (2016b) Biochemical and molecular characterization of salt-induced poor grain filling in a rice cultivar. Functional Plant Biology 43, 266–277.
Biochemical and molecular characterization of salt-induced poor grain filling in a rice cultivar.Crossref | GoogleScholarGoogle Scholar | 32480459PubMed |

Panda BB, Sekhar S, Dash SK, Behera L, Shaw BP (2018) Biochemical and molecular characterisation of exogenous cytokinin application on grain filling in rice. BMC Plant Biology 18, 89
Biochemical and molecular characterisation of exogenous cytokinin application on grain filling in rice.Crossref | GoogleScholarGoogle Scholar | 29783938PubMed |

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 Y (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 |

Pettkó-Szandtner A, Cserháti M, Barrôco RM, Hariharan S, Dudits D, Beemster GTS (2015) Core cell cycle regulatory genes in rice and their expression profiles across the growth zone of the leaf. Journal of Plant Research 128, 953–974.
Core cell cycle regulatory genes in rice and their expression profiles across the growth zone of the leaf.Crossref | GoogleScholarGoogle Scholar | 26459328PubMed |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |

Qi P, Lin Y-S, Song X-J, Shen J-B, Huang W, Shan J-X, Zhu M-Z, Jiang L, Gao J-P, Lin H-X (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Research 22, 1666–1680.
The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3.Crossref | GoogleScholarGoogle Scholar | 23147796PubMed |

Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiology 149, 14–26.
The development of endosperm in grasses.Crossref | GoogleScholarGoogle Scholar | 19126691PubMed |

Sabelli PA, Leiva-Neto JT, Dante RA, Nguyen H, Larkins BA (2005) Cell cycle regulation during maize endosperm development. Maydica 50, 485–496.

Sabelli PA, Dante RA, Hong N, Nguyen HN, Gordon-Kamm WJ, Larkins BA (2014) Expression, regulation and activity of a B2-type cyclin in mitotic and endoreduplicating maize endosperm. Frontiers in Plant Science 5, 561
Expression, regulation and activity of a B2-type cyclin in mitotic and endoreduplicating maize endosperm.Crossref | GoogleScholarGoogle Scholar | 25368625PubMed |

Sekhar S, Panda BB, Mohapatra T, Das K, Shaw BP, Kariali E, Mohapatra PK (2015a) 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) 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) cultivars.Crossref | GoogleScholarGoogle Scholar | 25817414PubMed |

Sekhar S, Gharat SA, Panda BB, Mohapatra T, Das K, Kariali Mohapatra PK, Shaw BP (2015b) Identification and characterization of differentially expressed genes in inferior and superior spikelets of rice cultivars with contrasting panicle-compactness and grain-filling properties. PLoS One 10, e0145749
Identification and characterization of differentially expressed genes in inferior and superior spikelets of rice cultivars with contrasting panicle-compactness and grain-filling properties.Crossref | GoogleScholarGoogle Scholar | 26710230PubMed |

Shimotohno A, Ohno R, Bisova K, Sakaguchi N, Huang J, Koncz C, Uchimiya H, Umeda M (2006) Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis. The Plant Journal 47, 701–710x.
Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16856985PubMed |

Singh BK, Jenner CF (1982) A modified method for determination of cell number in wheat endosperm. Plant Science Letters 26, 273–278.
A modified method for determination of cell number in wheat endosperm.Crossref | GoogleScholarGoogle Scholar |

Stein O, Granot D (2019) An overview of sucrose synthase in plants. Frontiers in Plant Science 10, 95
An overview of sucrose synthase in plants.Crossref | GoogleScholarGoogle Scholar | 30800137PubMed |

Ta KN, Khong NG, Ha TL, Nguyen DT, Mai DC, Hoang TG, Phung TPN, Bourrie I, Courtois B, Tran TTH, Dinh BY, La TN, Do NV, Lebrun M, Gantet P, Jouannic S (2018) A genome-wide association study using a Vietnamese landrace panel of rice (Oryza sativa) reveals new QTLs controlling panicle morphological traits. BMC Plant Biology 18, 282
A genome-wide association study using a Vietnamese landrace panel of rice (Oryza sativa) reveals new QTLs controlling panicle morphological traits.Crossref | GoogleScholarGoogle Scholar | 30428844PubMed |

Umeda M, Umeda-Hara C, Yamaguchi M, Hashimoto J, Uchimiya H (1999a) Differential expression of genes for cyclin-dependent protein kinases in rice plants. Plant Physiology 119, 31–40.
Differential expression of genes for cyclin-dependent protein kinases in rice plants.Crossref | GoogleScholarGoogle Scholar | 9880343PubMed |

Umeda M, Iwamoto N, Umeda-Hara C, Yamaguchi M, Hashimoto J, Uchimiya H (1999b) Molecular characterization of mitotic cyclins in rice plants. Molecular & General Genetics 262, 230–238.
Molecular characterization of mitotic cyclins in rice plants.Crossref | GoogleScholarGoogle Scholar |

Umeda M, Shimotohno A, Yamaguchi M (2005) Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant & Cell Physiology 46, 1437–1442.
Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants.Crossref | GoogleScholarGoogle Scholar |

UN (United Nations) (2013) World population prospects: the 2012 revision. Department of Economic and Social Affairs, Population Division, UN, New York. Working Paper No. ESA/P/WP.228;2013. Available at http://esa.un.org/unpd/wpp/publications/Files/WPP2012_HIGHLIGHTS.pdf [Verified 28 September 2020]

Venkateswarlu B, Vergara BS, Parao FT, Visperas RM (1986) Enhanced grain yield potentials in rice by increasing the number of high density grains. Philippine Journal of Crop Science 11, 145–152.

Virk PS, Khush GS, Peng S (2004) Breeding to enhance yield potential of rice at IRRI: the ideotype approach. International Rice Research Notes 29, 5–9.

Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, dePamphilis CW, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiology 135, 1084–1099.
Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins.Crossref | GoogleScholarGoogle Scholar | 15208425PubMed |

Wang F, Cheng F, Zhang G (2008a) Impact of cultivar variation in grain density of rice panicle on grain weight and quality. Journal of the Science of Food and Agriculture 88, 897–903.
Impact of cultivar variation in grain density of rice panicle on grain weight and quality.Crossref | GoogleScholarGoogle Scholar |

Wang H, Zhou Y, Bird DA, Fowke LC (2008b) Functions, regulation and cellular localization of plant cyclin-dependent kinase inhibitors. Journal of Microscopy 231, 234–246.
Functions, regulation and cellular localization of plant cyclin-dependent kinase inhibitors.Crossref | GoogleScholarGoogle Scholar | 18778421PubMed |

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 |

Weingartner M, Criqui M-C, Tamas M, Binarova P, Schmit A-C, Helfer A, Derevier A, Erhardt M, Borge L, Genschik P (2004) Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast. The Plant Cell 16, 643–657.
Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast.Crossref | GoogleScholarGoogle Scholar | 15004270PubMed |

Yamaguchi M, Fabian T, Sauter M, Bhalerao RP, Schrader J, Sandberg G, Umeda M, Uchimiya H (2000) Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants. The Plant Journal 24, 11–20.
Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants.Crossref | GoogleScholarGoogle Scholar | 11029700PubMed |

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 |

Yang J, Peng S, Zhang Z, 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, 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 |

Yi D, Kamei CL, Cools T, Vanderauwera S, Takahashi N, Okushima Y, Eekhout T, Yoshiyama KO, Larkin J, den Daele HV, Cocklin P, Britt A, Umeda M, De Veylder L (2014) The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. The Plant Cell 26, 296–309.
The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 24399300PubMed |

Yin X, Gourdriaan J, Lantinga EA, Vos J, Spiertz HJ (2003) A flexible sigmoid function of determinate growth. Annals of Botany 91, 361–371.
A flexible sigmoid function of determinate growth.Crossref | GoogleScholarGoogle Scholar | 12547689PubMed |

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 W (2014) A proteomic study on molecular mechanism of poor grain-filling of rice (Oryza sativa L.) inferior spikelets. PLoS One 9, e89140

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

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.