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

Biochemical and molecular characterisation of salt-induced poor grain filling in a rice cultivar

Binay B. Panda A , Alok K. Badoghar A , Sudhanshu Sekhar A , Ekamber Kariali B , Pravat K. Mohapatra B and Birendra P. Shaw A C
+ Author Affiliations
- Author Affiliations

A Environmental Biotechnology Laboratory, Institute of Life Sciences, Nalco Square, Bhubaneswar-751023, Odisha, India.

B School of Life Sciences, Sambalpur University, Sambalpur, 768019, Odisha, India.

C Corresponding author. Email: bpshaw@ils.res.in

Functional Plant Biology 43(3) 266-277 https://doi.org/10.1071/FP15229
Submitted: 4 August 2015  Accepted: 6 November 2015   Published: 15 December 2015

Abstract

Despite the prevalence of poor grain filling in rice (Oryza sativa L.) under abiotic stress, the reason for this is largely unexplored. Application of 0.75% NaCl to a salt-sensitive rice cultivar at late booting resulted in a >20% yield loss. Spikelets per panicle and the percentage of filled grain decreased significantly in response to NaCl application. The inhibitory effect of NaCl on grain filling was greater in basal than in apical spikelets. Sucrose synthase (SUS) activity was positively correlated with grain weight. The transcript levels of the SUS isoforms differed greatly: the levels of SUS2 increased significantly in response to salt; those of SUS4 decreased drastically. Gene expression studies of starch synthase and ADP-glucose pyrophosphorylase showed that the decreased transcript levels of one isoform was compensated by an increase in those of the other. Salt application also significantly increased the gene expression of the ethylene receptors and the ethylene signalling proteins. The increase in their transcript levels was comparatively greater in basal than in apical spikelets. Significant enhancement in the transcript levels of the ethylene receptors and the increase in the production of ethylene indicated that the salt-induced inhibition of grain filling might be mediated by ethylene. Additionally, the inhibition of chromosomal endoreduplication mediated by decreased transcript levels of B-type cyclin could explain poor grain filling under salt stress. A significant increase in the transcript levels of the ethylene-responsive factors in the spikelets during grain filling in response to salt indicated their possible protective role in grain filling under stress.

Additional keywords: abiotic stress, chromosomal endoreduplication, ethylene receptor,NaCl salinity, Oryza sativa, sucrose synthase.


References

Abdullah Z, Khan MA, Flowers TJ (2001) Causes of sterility in seed set of rice under salinity stress. Journal Agronomy & Crop Science 187, 25–32.
Causes of sterility in seed set of rice under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Akbar M, Ponnamperuma FN (1982) Saline soils of south and Southeast Asia as potential rice lands. In ‘Rice research strategies for the future’. (Eds WG Rockwood, C Mendoza) pp. 265–281. (International Rice Research Institute: Manila)

Asch F, Wopereis MCS (2001) Responses of field-grown irrigated rice cultivars to varying levels of floodwater salinity in a semi-arid environment. Field Crops Research 70, 127–137.
Responses of field-grown irrigated rice cultivars to varying levels of floodwater salinity in a semi-arid environment.Crossref | GoogleScholarGoogle Scholar |

Beltrano J, Carbone A, Montaldi ER, Guiamet JJ (1994) Ethylene as promoter of wheat grain maturation and ear senescence. Plant Growth Regulation 15, 107–112.
Ethylene as promoter of wheat grain maturation and ear senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1KmtL4%3D&md5=30afcddd78373a6ed23e5764f0451ea6CAS |

Bhatia S, Singh R (2002) Phytohormone-mediated transformation of sugars to starch in relation to the activities of amylases, sucrose-metabolising enzymes in sorghum grain. Plant Growth Regulation 36, 97–104.
Phytohormone-mediated transformation of sugars to starch in relation to the activities of amylases, sucrose-metabolising enzymes in sorghum grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtlGlt7g%3D&md5=227570f5e430a63fc68a621457211f1fCAS |

Bradford M (1976) A rapid and sensitive method for quantitation of microgram of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for quantitation of microgram of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=0c5b9be40df67b5bda977fd44a3222a3CAS | 942051PubMed |

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-Chhetri) pp. 326–345. (Birkhäuser: Basel)

Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Frontiers in Plant Science 5, 1–14.
Cell cycle control and seed development.Crossref | GoogleScholarGoogle Scholar |

Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiology 136, 2457–2462.
Sodium transporters in plants. Diverse genes and physiological functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrtbg%3D&md5=1e6c474259eabc209edb206cb4564ed6CAS | 15375202PubMed |

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 |

Ju C, Chang C (2012) Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. AoB Plants 2012, pls031
Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane.Crossref | GoogleScholarGoogle Scholar | 23119138PubMed |

Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287–291.
Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1Chu78%3D&md5=5f12e5c960dc5f074361bfc66e2c069fCAS | 10096298PubMed |

Kumar V, Singh A, Mithra SVA, Krishnamurthy SL, Parida SK, Jain S, Tiwari KK, Kumar P, Rao AR, Sharma SK, Khurana JP, Singh NK, Mohapatra T (2015) Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Research 22, 133–145.
Genome-wide association mapping of salinity tolerance in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 25627243PubMed |

Lei G, Shen M, Li ZG, Zhang B, Duan KX, Wang N, Cao YR, Zhang WK, Ma B, Ling HQ, Chen SY, Zhang JS (2011) EIN2 regulates salt stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis. Plant, Cell & Environment 34, 1678–1692.
EIN2 regulates salt stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlarurnN&md5=e324d130bde0ebabd95ce86ec3c9c763CAS |

Mészáros T, Miskolczi P, Ayaydin F, Pettko-Szandtner A, Peres A, Magyar Z, Horvath GV, Bako L, Feher A, Dudits D (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Molecular Biology 43, 595–605.
Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells.Crossref | GoogleScholarGoogle Scholar | 11089863PubMed |

Mizutani M, Naganuma T, Tsutsumi KI, 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 | 1:CAS:528:DC%2BC3cXhsVSrtL0%3D&md5=cb43f0b7c852c7af27436d5401f4af2fCAS | 19933315PubMed |

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 | 1:CAS:528:DC%2BD1cXhsFagtbvI&md5=8cc3c3cf9238fa8ab7d954c5169baf0bCAS |

Myers PN, Setter TL, Madison JT, Thompson JF (1990) Abscisic acid inhibition of endosperm cell division in cultured maize kernels. Plant Physiology 94, 1330–1336.
Abscisic acid inhibition of endosperm cell division in cultured maize kernels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjsFyj&md5=06374b623f8b3a46ddefd69f29c39899CAS | 16667837PubMed |

Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiology 150, 1368–1379.
Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFertbY%3D&md5=68b9024498381284e55af104b043c5aaCAS | 19429605PubMed |

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 | 1:CAS:528:DC%2BD1MXltlKkurw%3D&md5=e29195bce32efd086792cb8442d5e04aCAS |

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 | 1:CAS:528:DC%2BC2MXhtlajtbrE&md5=cdf29be245b437273aef58c2f9b7ffe6CAS |

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 | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=eb0e45d55c793e8429a09a6f6eb7babbCAS | 11328886PubMed |

Rad HE, Aref F, Rezaei M (2012) Response of rice to different salinity levels during different growth stages. Research Journal of Applied Science Engineering and Technology 4, 3040–3047.

Rao PS, Mishra B, Gupta SR (2013) Effects of soil salinity and alkalinity on grain quality of tolerant, semi-tolerant and sensitive rice genotypes. Rice Science 20, 284–291.
Effects of soil salinity and alkalinity on grain quality of tolerant, semi-tolerant and sensitive rice genotypes.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) 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 | 1:CAS:528:DC%2BC2MXkvVSrtbc%3D&md5=e2fbb862ffd3cc83e4e6c16be2c1625bCAS | 25817414PubMed |

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 |

Thitisaksakul M, Tananuwong K, Shoemaker CF, Chun A, Tanadul OU, Labavitch JM, Beckles DM (2015) Effects of timing and severity of salinity stress on rice (Oryza sativa L.) yield, grain composition, and starch functionality. Journal of Agricultural and Food Chemistry 63, 2296–2304.
Effects of timing and severity of salinity stress on rice (Oryza sativa L.) yield, grain composition, and starch functionality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtl2js7g%3D&md5=6a3ef12087ef7b800f18090e1cfb7080CAS | 25615402PubMed |

Valente P, Tao W, Verbelen JP (1998) Auxins and cytokinins control DNA endoreduplication and deduplication in single cells of tobacco. Plant Science 134, 207–215.
Auxins and cytokinins control DNA endoreduplication and deduplication in single cells of tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXks1Omsrc%3D&md5=c592cf0cf92581f5862a01e2c1472392CAS |

Wan L, Zhang J, Zhang H, Zhang Z, Quan R, Zhou S, Huang R (2011) Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS One 6, e25216
Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtleis7nF&md5=391ef6ab6b3d4cd67183459ceb949fbcCAS | 21966459PubMed |

Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, Jiang L, Guo H (2012) Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Research 22, 1613–1616.
Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1arsLjO&md5=ca9921ec80251edc8a442bb6155d99d3CAS | 23070300PubMed |

Wuriyanghan H, Zhang B, Cao WH, Ma BA, Lei G, Liu YF, Wei W, Wu HJ, Chen LJ, Chen HW, Cao YR, He SJ, Zhang WK, Wang XJ, Chen SY, Zhang JS (2009) The ethylene receptor etr2 delays floral transition and affects starch accumulation in rice. The Plant Cell 21, 1473–1494.
The ethylene receptor etr2 delays floral transition and affects starch accumulation in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVCqtL4%3D&md5=20565f294837dca4b0f3c04a46243135CAS | 19417056PubMed |

Zeng L, Shannon MC (2000) Salinity effects on seedling growth and yield components of rice. Crop Science 40, 996–1003.
Salinity effects on seedling growth and yield components of rice.Crossref | GoogleScholarGoogle Scholar |

Zeng L, Shannon MC, Lesch SM (2001) Timing of salinity stress effects rice growth and yield components. Agricultural Water Management 48, 191–206.
Timing of salinity stress effects rice growth and yield components.Crossref | GoogleScholarGoogle Scholar |

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 | 1:CAS:528:DC%2BC3MXptFCqur4%3D&md5=88394fc933fe98450f25c8bf13aaa859CAS | 21459770PubMed |