Screening for Spikelet Fertility and Validation of Heat Tolerance in a Large Rice Mutant Population

doi:10.1016/j.rsci.2018.08.008

Abstract

Abstract:

A total of 10 000 M₄ individuals in Jao Hom Nil (JHN) mutant population was treated with high temperature (40 ºC to 45 ºC) during the day time (6 h) from the booting to the harvesting stages, and ambient temperature (33 ºC to 35 ºC) was used as the control. The results of screening and yield trials found that the mutant line M9962 had a high spikelet fertility of 78% under heat stress. In addition, the other mutant lines, including M3181 and M7988, had a spikelet fertility of approximately 70%. However, the JHN wild type, Sin Lek, RD15 and RD33 had very low spikelet fertility of 34%, 14%, 9% and 4%, respectively. The lower spikelet fertility at an elevated temperature resulted in a dramatic decrease of filled grain and contributed to a loss in 100-grain weight. M9962 is a potential genetic stock for use in a heat tolerance breeding programme. In addition, spikelet fertility at high temperature was representative of heat tolerance and can be used as a screening trait for heat tolerance during the reproductive phase on a large scale.

Key words: high temperature, rice, spikelet fertility, heat tolerance, mutant

Cheabu Sulaiman, Panichawong Nat, Rattanametta Prisana, Wasuri Boonthong, Kasemsap Poonpipope, Arikit Siwaret, Vanavichit Apichart, Malumpong Chanate. Screening for Spikelet Fertility and Validation of Heat Tolerance in a Large Rice Mutant Population[J]. Rice Science, 2019, 26(4): 229-238.

Figures/Tables 12

References 45

[1]	Ahloowalia B S, Maluszynski M, Nichterlein K.2004. Global impact of mutation-derived varieties.Euphytica, 135(2): 187-204.
[2]	Baker J T, Allen Jr L H, Boote K J.1992. Temperature effects on rice at elevated CO2 concentration.J Exp Bot, 43: 959-964.
[3]	Chakhonkaen S, Pitnjam K, Saisuk W, Ukoskit K, Muangprom A.2012. Genetic structure of Thai rice and rice accessions obtained from the International Rice Research Institute.Rice, 5(1): 19.
[4]	Chumpolsri W, Wijit N, Boontakham P, Nimmanpipug P, Sookwong P, Luangkamin S, Wongpornchai S.2015. Variation of terpenoid flavor odorants in bran of some black and white rice varieties analyzed by GC × GC-MS.J Food Nutr Res, 3(2): 114-120.
[5]	Counce P A, Keisling T C, Mitchell A J.2000. A uniform, objective, and adaptive system for expressing rice development.Crop Sci, 40(2): 436-443.
[6]	Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M.2009. High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development.Plant Cell Physiol, 50(11): 1911-1922.
[7]	González-Schain N, Dreni L, Lawas L M F, Galbiati M, Colombo L, Heuer S, Jagadish K S V, Kater M M.2015. Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties.Plant Cell Physiol, 57(1): 57-68.
[8]	Huang L Y, Sun Y, Peng S B, Wang F.2016. Genotypic differences ofjaponica rice responding to high temperature in China. Agron J, 108(2): 626-636.
[9]	IPCC. 2014. Climate Change 2013: The Physical Science Basis. Cambridge, and New York: Cambridge University Press.
[10]	IRRI.2013. Standard Evaluation System for Rice (SES). Manila, the Philippines:International Rice Research Institute. 5: 35-36.
[11]	Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh Y A, Yoshinaga S, Ando I, Ogawa T, Kondo M.2010. A genetic resource for early-morning flowering trait of wild riceOryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Ann Bot, 106(3): 515-520.
[12]	Jagadish S V K, Craufurd P Q, Wheeler T R.2007. High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot, 58(7): 1627-1635.
[13]	Jagadish S V K, Craufurd P Q, Wheeler T R.2008. Phenotyping parents of mapping populations of rice for heat tolerance during anthesis.Crop Sci, 48(3): 1140-1146.
[14]	Jagadish S V K, Muthurajan R, Oane R, Wheeler T R, Heuer S, Bennett J, Craufurd P Q.2010. Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J Exp Bot, 61(1): 143-156.
[15]	Kobayashi K, Matsui T, Murata Y, Yamamoto M.2011. Percentage of dehisced thecae and length of dehiscence control pollination stability of rice cultivars at high temperatures.Plant Prod Sci, 14(2): 89-95.
[16]	Lee I S, Kim D S, Lee S J, Song H S, Lim Y P, Lee Y I.2003. Selection and characterizations of radiation-induced salinity- tolerant lines in rice.Breeding Sci, 53(4): 313-318.
[17]	Manigbas N L, Lambio L A F, Madrid L B, Cardenas C C.2014. Germplasm innovation of heat tolerance in rice for irrigated lowland conditions in the Philippines.Rice Sci, 21(3): 162-169.
[18]	Maruyama A, Weerakoon W M W, Wakiyama Y, Ohba K.2013. Effects of increasing temperatures on spikelet fertility in different rice cultivars based on temperature gradient chamber experiments.J Agron Crop Sci, 199(6): 416-423.
[19]	Masuduzzaman A S M, Ahmad H U, Haque M, Ahmed M M E.2016. Evaluation of rice lines tolerant to heat during flowering stage.J Rice Res, 4: 170.
[20]	Matsui T, Namuco O S, Ziska L H, Horie T.1997. Effects of high temperature and CO2 concentration on spikelet sterility inindica rice. Field Crops Res, 51(3): 213-219.
[21]	Matsui T, Omasa K, Horie T.2000. High temperature at flowering inhibits swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.). Plant Prod Sci, 3(4): 430-434.
[22]	Matsui T, Omasa K, Horie T.2001. The difference in sterility due to high temperatures during the flowering period amongjaponica-rice varieties. Plant Prod Sci, 4(2): 90-93.
[23]	Matsui T, Omasa K.2002. Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: Anther characteristics. Ann Bot, 89(6): 683-687.
[24]	Miyagawa S.2001. Dynamics of rainfed lowland rice varieties in north-east Thailand. In: Saxena K G. Small-Scale Livelihoods and Natural Resource Management in Marginal Areas ofMonsoon Asia. Cornell University.
[25]	Mohapatra T, Robin S, Sarla N, Sheshashayee M, Singh A K, Singh K, Singh N K, Amitha Mithra S V, Sharma R P.2014. EMS induced mutants of upland rice variety Nagina 22: Generation and characterization.Proc Ind Nat Sci Acad, 80(1): 163-172.
[26]	Moung-ngam P.2016. Evaluation of Heat Tolerance in Rice Germplasm. [Master thesis]. Bangkok, Thailand:Kasetsart University.
[27]	Moya T B, Ziska L H, Namuco O S, Olszyk D.1998. Growth dynamics and genotypic variation in tropical, field-grown paddy rice (Oryza sativa L.) in response to increasing carbon dioxide and temperature. Global Change Biol, 4(6): 645-656.
[28]	Nakagawa H, Horie T, Matsui T.2003. Effects of Climate Change on Rice Production and Adaptive Technologies. Manila,the Philippines: International Rice Research Institute: 635-658.
[29]	Napasintuwong O.2012. Survey of recent innovations in aromatic rice. In: The 131st EAAE Seminar ‘Innovation for Agricultural Competitiveness and Sustainability of Rural Areas’. September 18-19, 2012. Prague,Czech Republic.
[30]	Peng S, Huang J, Sheehy J E, Laza R C, Visperas R M, Zhong X, Centeno G S, Khush G S, Cassman K G.2004. Rice yields decline with higher night temperature from global warming.Proc Natl Acad Sci USA, 101: 9971-9975.
[31]	Poli Y, Basava R K, Panigrahy M, Vinukonda V P, Dokula N R, Voleti S R, Desiraju S, Neelamraju S.2013. Characterization of a Nagina 22 rice mutant for heat tolerance and mapping of yield traits.Rice, 6(1): 36.
[32]	Prasad P V V, Boote K J, Allen L H, Sheehy J E, Thomas J M G.2006. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress.Field Crops Res, 95: 398-411.
[33]	Prasanth V V, Basava K R, Babu M S, Venkata Tripura V G N, Rama Devi S J S, Mangrauthia S K, Voleti S R, Sarla N.2016. Field level evaluation of rice introgression lines for heat tolerance and validation of markers linked to spikelet fertility.Physiol Mol Biol Plants, 22(2): 179-192.
[34]	Rang Z W, Jagadish S V K, Zhou Q M, Craufurd P Q, Heuer S.2011. Effect of high temperature and water stress on pollen germination and spikelet fertility in rice.Environ Exp Bot, 70(1): 58-65.
[35]	Ruengphayak S, Ruanjaichon V, Saensuk C, Phromphan S, Tragoonrung S, Kongkachuichai R, Vanavichit A.2015. Forward screening for seedling tolerance to Fe toxicity reveals a polymorphic mutation in ferric chelate reductase in rice.Rice, 8(1): 3.
[36]	Saleem M Y, Mukhtar Z, Cheema A A, Atta B M.2005. Induced mutation andin vitro techniques as a method to induce salt tolerance in Basmati rice(Oryza sativa L.). Int J Environ Sci Technol, 2(2): 141-145.
[37]	Satake T, Yoshida S.1978. High temperature-induced sterility inindica rices at flowering. Jpn J Crop Sci, 47(1): 6-17.
[38]	Shah F, Huang J L, Cui K H, Nie L M, Shah T, Chen C, Wang K.2011. Impact of high-temperature stress on rice plant and its traits related to tolerance.J Agric Sci, 149(5): 545-556.
[39]	Shi W J, Ishimaru T, Gannaban R B, Oane W, Jagadish S V K.2015. Popular rice (L.) cultivars show contrasting responses to heat stress at gametogenesis and anthesis.Crop Sci, 55(2): 589-596.
[40]	Sukkeoa S, Rerkasemb B, Jamjoda S.2017. Heat tolerance in Thai rice varieties.Sci Asia, 43(2): 61-69.
[41]	Tenorio F A, Ye C, Redoña E, Sierra S, Laza M, Argayoso M A2013. Screening rice genetic resources for heat tolerance.SABRAO J Breeding Genet, 45(3): 371-381.
[42]	Wassmann R, Jagadish S V K, Sumfleth K, Pathak H, Howell G, Ismail A, Serraj R, Redona E, Singh R K, Heuer S.2009. Regional vulnerability of climate change impacts on Asian rice production and scope for adaptation.Adv Agron, 102: 91-133.
[43]	Wu Y J, Chen Y, Wang J, Zhu C X, Xu B L.2006. RAPD analysis of jasmine rice-specific genomic structure.Genome, 49(6): 716-719.
[44]	Ye C R, Argayoso M A, Redona E D, Sierra S N, Laza M A, Dilla C J, Mo Y J, Thomson M J, Chin J, Delaviña C B, Diaz G Q, Hernandez J E.2012. Mapping QTL for heat tolerance at flowering stage in rice using SNP markers.Plant Breeding, 131(1): 33-41.
[45]	Ziska L H, Manalo P A, Ordonez R A.1996. Intraspecific variation in the response of rice (Oryza sativa L.) to increased CO2 and temperature: Growth and yield response of 17 cultivars. J Exp Bot, 47(9): 1353-1359.

Experiment	Duration	Greenhouse
		Day time (6 h)				Night time
		T (^oC)	RH (%)	LI [µmol/(L·m²·s)]		T (^oC)	RH (%)
Preliminary screening	April-December 2012	41.70 ± 1.90	56.52 ± 4.42	1 001.17	29.07 ± 2.28		82.18 ± 4.90
Repeat screening	April-May 2013	42.13 ± 1.15	61.51 ± 4.47	929.26	29.41 ± 1.10		86.34 ± 4.85
Validation screening	July-August 2013	41.44 ± 1.62	59.10 ± 3.44	997.34	28.35 ± 1.20		84.57 ± 5.86
Experiment	Duration	In field
		Day time (6 h)				Night time
		T (^oC)	RH (%)	LI [µmol/(L·m²·s)]		T (^oC)	RH (%)
Preliminary screening	April-December 2012	35.42 ± 2.90	47.61 ± 7.76	1 667.13	28.68 ± 2.31		80.42 ± 6.49
Repeat screening	April-May 2013	35.24 ± 1.16	56.38 ± 5.81	1 468.89	27.97 ± 0.86		85.37 ± 7.01
Validation screening	July-August 2013	33.25 ± 1.26	55.37 ± 6.13	1 538.70	27.08 ± 0.95		83.45 ± 8.57

Experiment	Duration	Greenhouse
		Day time (6 h)				Night time
		T (^oC)	RH (%)	LI [µmol/(L·m²·s)]		T (^oC)	RH (%)
Preliminary screening	April-December 2012	41.70 ± 1.90	56.52 ± 4.42	1 001.17	29.07 ± 2.28		82.18 ± 4.90
Repeat screening	April-May 2013	42.13 ± 1.15	61.51 ± 4.47	929.26	29.41 ± 1.10		86.34 ± 4.85
Validation screening	July-August 2013	41.44 ± 1.62	59.10 ± 3.44	997.34	28.35 ± 1.20		84.57 ± 5.86
Experiment	Duration	In field
		Day time (6 h)				Night time
		T (^oC)	RH (%)	LI [µmol/(L·m²·s)]		T (^oC)	RH (%)
Preliminary screening	April-December 2012	35.42 ± 2.90	47.61 ± 7.76	1 667.13	28.68 ± 2.31		80.42 ± 6.49
Repeat screening	April-May 2013	35.24 ± 1.16	56.38 ± 5.81	1 468.89	27.97 ± 0.86		85.37 ± 7.01
Validation screening	July-August 2013	33.25 ± 1.26	55.37 ± 6.13	1 538.70	27.08 ± 0.95		83.45 ± 8.57

Score	Spikelet fertility	Description
1	> 80%	Highly tolerant
3	61%-80%	Tolerant
5	41%-60%	Moderately tolerant
7	11%-40%	Susceptible
9	< 11%	Highly susceptible

Score	Spikelet fertility	Description
1	> 80%	Highly tolerant
3	61%-80%	Tolerant
5	41%-60%	Moderately tolerant
7	11%-40%	Susceptible
9	< 11%	Highly susceptible

Cultivar	Origin	Grain type	Special trait
Dawk Pa-yawm	Native rice	Long	Upland rice
Homcholasit	RGDU*	Long	submergence tolerance
Jao Hom Nil	RGDU	Medium	Wild Type
Pathum Thani 1	Rice Department.	Long	Good quality
Pin Kaset 1	RGDU	Long	High yield
Pin Kaset 2	RGDU	Medium	High yield
Pin Kaset 3	RGDU	Long	High yield
PSL2	Rice Department.	Medium	Commercial cultivar
RD15	Rice Department.	Medium	Adaptable to drought
RD33	Rice Department.	Long	Blast resistance
Suphan Buri 1	Rice Department.	Medium	Commercial cultivar
Thanyasirin	RGDU	Medium	Waxy rice
A5029	RGDU	Long	Very long grain
Sinlek	RGDU	Long	Control for high temperature sensitivity
* RGDU; Rice gene discovery unit