JXB Advance Access originally published online on September 9, 2003
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Journal of Experimental Botany, Vol. 54, No. 392, pp. 2579-2585,
November 1, 2003
© 2003 Oxford University Press
Mapping of QTLs associated with cold tolerance during the vegetative stage in rice
Received 30 December 2002; Accepted 18 June 2003
1 Department of Agronomy and Range Science, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA
2 Plant Breeding, Genetics and Biochemistry Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines
* To whom correspondence should be addressed. Fax: +63 2 845 0606. E-mail: d.mackill{at}cgiar.org
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Abstract |
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Low-temperature stress is an important factor affecting the growth and development of rice (Oryza sativa L.) in temperate and high-elevation areas. Cold stress may cause various seedling injuries, delayed heading and yield reduction due to spikelet sterility. In this study, 181 microsatellite marker loci were used to identify quantitative trait loci (QTLs) associated with cold tolerance at the vegetative stage in 191 recombinant inbred lines (RILs) derived from a cross of a cold-tolerant temperate japonica cultivar (M-202) with a cold-sensitive indica cultivar (IR50). Different temperature regimes were applied in growth chambers on 191 RILs. The temperature regimes imposed in the growth chamber simulated cold-stress injuries at the seedling and late vegetative stages. In this study a major QTL was identified on chromosome 12, designated as qCTS12a, that was closely associated with cold-induced necrosis and wilting tolerance, and accounted for 41% of the phenotypic variation. A number of QTLs with smaller effects were also detected on eight rice chromosomes.
Key words: Abiotic stress, cold tolerance, QTL mapping, rice.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Low-temperature stress is common for rice (Oryza sativa L.) cultivation in temperate zones and high-elevation environments. An important breeding objective of these regions is to develop cultivars tolerant to low temperatures at critical growth stages (Nakagahra et al., 1997). In parts of south and south-east Asia, an estimated 7 000 000 hectares cannot be planted with modern varieties because of low-temperature stress (Sthapit and Witcombe, 1998). In temperate-growing regions such as California (USA), cold temperature is an important stress that results in delayed heading or maturation and yield reduction due to spikelet sterility (Peterson et al., 1974). Rice cultivars vary greatly in their tolerance to low temperature. The indica rice subspecies, associated with tropical environments, is more sensitive to low temperature. The more tolerant japonica subspecies is divided into tropical and temperate groups (Glaszmann, 1987; Glaszmann et al., 1990; Oka, 1988).
During the early growth stages in rice, the occurrence of low-temperature stress affects seed germination that inhibits seedling establishment and eventually leads to non-uniform crop maturation. Rice plants are injured at the seedling stage when they are grown in early spring in temperate or subtropical environments. In a survey conducted by Kaneda and Beachell (1974), the types of low-temperature effects on seedlings can be manifested as poor germination, slow growth, discoloration or yellowing, withering after transplanting, reduced tillering, and stunted growth.
Screening for chilling sensitivity of different rice genotypes in breeding programmes commonly relies on visual observations under natural field conditions. However, this type of screening is subject to genotypexenvironment interactions and diurnal or random fluctuations throughout the growing season and over years. Methods were also developed to assess cold tolerance under controlled conditions. These include chlorophyll fluorescence analysis (Sthapit et al., 1995), chilling survival tests using 10 °C at the two-leaf stage (Bertin et al., 1996), measurement of oxygen-scavenging enzymes (Saruyama and Tanida, 1995), ABA or polyamines (Lee et al., 1993, 1995), measurement of radicle growth (Saltveit, 2001) or seedling vigour (Redoña and Mackill, 1996). In addition to these methods, a molecular approach measures mRNA derived from seedlings exposed to chilling temperatures (Yoshida and Kato, 1994).
The diversity of symptoms of chilling injury in the various plant organs of sensitive species makes it difficult to find a single explanation of cellular events associated with tolerance. It was hypothesized that rices with low-temperature adaptation may maintain a greater capacity for phosphorylation of the light-harvesting protein complex of PSII (Gesch and Heilman, 1999). Since the symptoms of chilling damage to photosynthesis depend on characteristics of the low-temperature treatment, such as the light level, it is necessary to determine which type of damage is important under natural conditions. The damage to the photosynthetic machinery of plants, subjected to different levels of chilling temperature, has been reviewed recently (Allen and Ort, 2001; Sonoike, 1998).
Previous studies have indicated that rice response to low-temperature stress is complex and certainly controlled by more than one gene. However, genetic studies have indicated that chilling injury expressed as leaf withering is controlled by a major gene designated Cts2(t) and expression of leaf chlorosis by a gene designated as Cts1(t) (Nagamine, 1991). Cts1(t) is a single dominant gene controlling resistance to leaf yellowing that was identified earlier using 10-d-old seedlings screened at 12 °C for 10 d (Kwak et al., 1984). Misawa et al. (2000) conducted quantitative trait loci (QTL) analysis for cold tolerance at the seedling stage by subjecting plants to a temperature of 4 °C for 3 d. They identified five QTLs that were associated with the low-temperature response, one each on chromosomes 1, 9 and 11, and two on chromosome 3. Kim et al. (2000) identified a QTL for cold sensitivity on rice chromosome 5. Previous results also indicate that QTLs controlling booting-stage-cold tolerance (Andaya and Mackill, 2003) were not associated with seedling cold tolerance.
The mapping population used in this study was derived from a cross between a cold-tolerant California japonica cultivar M-202 and a cold-susceptible indica cultivar IR50 to locate QTLs responsible for cold tolerance at seedling stage. A growth chamber was used to simulate several cold-stress injuries and symptoms at the seedling or vegetative growth stage at different temperature regimes, and QTLs involved in their expression were identified.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Mapping population and microsatellite marker analysis
The derivation of the population used in mapping cold tolerance and marker analysis was as described in Andaya and Mackill (2003). A cross between M-202 and IR50 was made to develop a recombinant inbred line population to map cold tolerance at the seedling and late vegetative stage. A mapping population of 191 recombinant inbred lines (RILs) in the F6 generation was used to test for cold tolerance using a growth chamber.
DNA was extracted from leaf tissues following the protocol as described by Mackill (1995). The protocol for the polymerase chain reaction (PCR) amplification was modified from Ni et al. (2001). The samples were prepared in 96-well plates in a reaction volume of 15 µl containing1.5 µl PCR buffer (20 mM TRIS pH 8.0, 50 mM KCl, 2.5 mM MgCl2, 0.1 mM EDTA, 1 mM DTT, 50% glycerol), 50 ng DNA, 330 nM of each microsatellite primer pair (Research Genetics, Huntsville, AL, USA), 250 µM of each dNTP 330 nM rhodamine dye-labelled fluorescent dUTP, and 0.6 units Taq polymerase. For the PCR performed in GeneAmp PCR System 9700 thermocycler (Perkin-Elmer), the conditions were as follows: 2 min hold at 95 °C; 25 cycles of 95 °C for 15 s, 55 °C for 1 min, 72 °C for 30 s; final extension step at 72 °C for 5 min. Protocols for electrophoresis using the ABI Prism 377 (Applied biosystems) DNA sequencer followed the manufacturer’s recommendations. Fragment analysis was performed using the GeneScan software (Applied Biosystems).
Cold-tolerance screening
Measurement of cold tolerance was done using a Conviron PGV36 (Controlled Environments Ltd., Winnipeg) walk-in growth chamber. Ten 400 W metal-halide lamps, ten 400 W high-pressure sodium lamps and 12 100 W incandescent bulbs, placed approximately 1.5 m above the chamber floor, provided the 12 h light period inside the growth chamber. The light intensity 60 cm above the floor was measured as 800 µmol m–2 s–1 while the relative humidity ranged from 75–85%. Two chambers were used for the experiment, one for each of the two temperature regimes for cold-tolerance screening at the seedling stage: (a) 9 °C constant day/night temperature, and (b) 25/9 °C day/night temperature regime.
The experiment was a randomized complete-block design with three replicates. The parental varieties were replicated 18 times to monitor the appearance of cold injury using nine germination trays (TLC Polyform Inc, MN, USA). Twelve seeds of each RIL were planted in Sunshine Mix No. 1 potting soil (SunGro, Bellevue, WA) on 23 July 2000. Seeds were allowed to germinate and grow until the 3-leaf stage in a growth chamber set at 25/20 °C day/night temperature, 12 h photoperiod. At 14 d after seeding, the growth chambers were adjusted to their respective low-temperature regimes.
For the 9 °C constant-temperature treatment, scoring was done at 8, 14, 16, and 18 d of treatment using the scale of 1 (tolerant, all leaves normal, no apparent visual injury) to 9 (susceptible, all leaves wilted, seedlings apparently dead) as described in the Standard Evaluation Systems in rice (Fig. 1A) (IRRI, 1988). Instead of expressing the trait as overall cold tolerance, it was expressed as cold-induced wilting tolerance (CIWT) since the primary symptom of injury was wilting or withering as observed under more severe temperature conditions (Nagamine, 1991). For the 25/9 °C day/night temperature treatment, measurements were taken at 14, 18, and 28 d of treatment, and a score of 1 indicated that the plants were tolerant, had normal leaf colour and no growth retardation, while a score of 9 indicated that the plants were susceptible, leaves turned yellow and overall growth was stunted (Fig. 1B). The trait was expressed as overall cold tolerance (CT).
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To study the expression of tolerance at the later growth stages, 60-d-old plants were subjected to a 12 °C constant temperature for 5 d. The results were expressed as cold-induced necrosis tolerance (CINT), where the injury was observed as necrotic spots on the stem and cold-induced yellowing tolerance (CIYT) observed in the leaves, measurement followed the scale of 1 (no necrosis, leaves green) to 9 (stem necrotic, leaves yellow).
QTL analysis
A total of 181 microsatellite marker loci were used in constructing the genetic map and in QTL analysis using the linkage software MAPMAKER 2.0 for the Macintosh computer (Lander et al., 1987). The final map had a total length of 1276.8 cM with the average distance between two markers of 7.1 cM.
The DOS-based program PLABQTL (Utz and Melchinger, 1996) was used for QTL analysis. To identify putative QTLs, the program performs composite interval mapping (Jansen and Stam, 1994; Zeng, 1994) by the multiple regression approach. The conditional expectations of QTL genotypes, given the observed marker genotypes at the flanking marker loci, were calculated according to Haley and Knott (1992) using selected markers as co-factors. Critical threshold values of LOD scores for QTL detection by composite-interval mapping were calculated using the chi-square approximation suggested by Zeng (1994) and are equivalent to LOD=3.52 and 4.22 at experiment-wise error of P=0.05 and 0.01, respectively. The percentage of the phenotypic variation explained by the QTL was expressed as R2 based on the output of the PLABQTL program.
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Phenotypic data
The RIL population exhibited all range of scores from 1–9 even at later scoring dates (Table 1). CINT scores could be classified as either susceptible (7–9) or tolerant (1–3), while CIYT was skewed towards the tolerant type (data not shown). Score distribution was normal for CT and CIWT at later scoring dates, although a greater number of RILs were categorized in the extreme classes. Correlation analysis indicated that the only significant relationship was between CINT and CIWT (r=0.76, P <0.01). Overall, the continuous distribution and higher frequency of parental classes indicated that major, as well as minor, genes contributed to the cold-tolerance traits.
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For all the cold-tolerance categories, M-202 retained its tolerant score at all scoring dates whereas IR50 was susceptible even in the early scoring periods. The scale used to score cold tolerance, based on the degree of wilting and necrosis (Fig. 1A) and degree of yellowing and stunting (Fig. 1B), approximated conditions where plants were exposed to a constant severe stress and a situation where stress was only experienced during the night. The ability of plants to recover after relief from stress is also an important characteristic of tolerant plants. However, the scoring for this trait was more difficult, and less reliable, and it was not used in subsequent analysis. One problem was that lines suffered varying degrees of damage depending on their tolerance to the stress, and this could have affected the recovery score.
The cold tolerance of rice at the seedling and late vegetative stage is difficult to measure in a single test because of the complexity of injuries and symptoms caused by low-temperature stress. Based on the visual symptoms and injuries induced during treatments at 9 °C constant temperature, 25/9 °C day/night temperature treatment and 12 °C constant-temperature regime at the late vegetative stage under varying scoring dates, cold tolerance could be classified by at least four measurements. CT was scored based on the visual scale at 25/9 °C regime that approximates a cool night and warm day. The seedlings treated under this condition did not reach wilting, withering or death, but suffered severe stunting and leaf yellowing as the duration of stress was prolonged. CIWT approximates the treatment condition and injury type observed by Nagamine (1991). IR50, being a susceptible tropical indica, started to develop the symptom as early as 7 d of treatment whereas M-202 could tolerate more than 18 d. Seedling wilt or withering and death could be a complex of dehydration or excessive necrosis leading to additional categories for cold tolerance, CINT and CIYT. These two categories were measured using older plants to provide a more accurate measurement than at seedling stage. Older plants exposed to cold stress showed damage quicker than the young seedlings. Since damage was more pronounced, it was easier to score tolerance, especially leaf colour differences and necrosis. Necrosis appeared as brown spots on the stem and yellowing of the leaves even for a treatment as short as 5 d at 12 °C constant temperature. Kwak et al. (1984) observed this injury type by using 10-d-old seedlings for a 10 d treatment at this temperature.
Identification of QTLs
The QTLs detected for the four cold-tolerance categories are presented in Table 2. In all traits, the critical LOD threshold calculated using the chi-square approximation was 3.52 and 4.22, at P=0.05 and 0.01, respectively. This threshold level is higher than the level of LOD=2.5 to 3.0 used in many other studies. The higher LOD threshold level was set to reduce false positives and to focus on the more significant QTLs with higher contribution to the phenotypic variation. For all QTLs detected, only three showed a positive effect of the allele from IR50 (Table 2).
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A major QTL (LOD=20.34) controlling CIWT was identified on chromosome 12 with an average contribution of 41% to the phenotypic variation (Table 2). The QTL, designated qCTS12a, was within a 3.8 cM interval flanked by RM101–RM292 proximal to the centromeric region. Four other minor QTLs, with individual contributions to the phenotypic variation ranging from 8.7 to 12.7, were identified.
Six QTLs on different chromosomes were identified that influenced CT, accounting for a total of 46% of the phenotypic variation (Table 2; Fig. 2). The QTL identified on chromosome 4, designated as qCTS4-1, accounted for about 21% of the phenotypic variation. This particular QTL was also responsible for tolerance to cold-induced stunting at 28 d of treatment, accounting for 30% of the phenotypic variation (data not shown). Since the scoring for CT was based on leaf yellowing and stunting of seedling growth, similar to the injury observed by Kwak et al. (1984), the results might suggest that one of these detected QTLs was the major gene Cts1(t), specifically the one identified on chromosome 4. The QTL qCTS1, appeared to map near one of the QTLs identified by Misawa et al. (2000) on rice chromosome 1.
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The regions on chromosomes 8 and 12 responsible for CIWT were also detected for CINT with an additional QTL on chromosome 11 that mapped near one of the loci identified by Misawa et al. (2000). For CIYT, a single QTL on chromosome 4 was identified that accounted for 14% of the phenotypic variation. Unlike wilting and necrosis, leaf yellowing as a visual manifestation of cool-temperature damage was more difficult to score and less precise. It also took a longer duration of stress before the symptoms were manifested, requiring that the trait be rated several times.
Since the intensity of cold stress corresponds to that used by Nagamine (1991), the major QTL on chromosome 12 flanked by RM101–RM292 is probably the Cts2(t) gene as reported earlier. This QTL was not involved in CT confirming the observation that a different set of genes are involved in tolerance to chilling-induced wilting and tolerance to leaf yellowing (Nagamine, 1991). Interest ingly, a relatively minor QTL for a percentage of undeveloped spikelets resulting from cold stress at the booting stage was found at this location (Andaya and Mackill, 2003).
Twelve regions on all chromosomes, except chromosomes 2, 5, 7, and 9, contributed to overall cold tolerance at the vegetative stage (Fig. 2). A region flanked by RM35–RM230 on the long arm of chromosome 8 controlled CT, CIWT and CINT. A major gene within the interval RM101-RM292 on chromosome 12 was associated with tolerance to wilting and necrosis. The QTL was particularly interesting because it was detected in seedlings as well as on older rice plants subjected to low-temperature stress. A QTL with a relatively small effect on undeveloped spikelets was observed at this locus in a previous study on tolerance at the booting stage using the same population (Andaya and Mackill, 2003). It is not known if this effect resulted from the same QTL.
At present, thousands of rice microsatellite markers (McCouch et al., 2002) are available commercially that would enhance the power of QTL mapping. If the new markers around the putative QTL regions prove to be polymorphic, it will be possible to identify closely-linked markers that may be used for marker-aided selection or for fine-mapping and ultimately cloning the genes of interest. Additional QTLs may also be detected if the large gaps on the genetic map are filled. A further addition of microsatellite markers on the target QTL regions is now underway.
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Conclusion |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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In this study, several QTLs associated with cold tolerance in rice were identified under a controlled-environment condition. Since the type of cold injury may vary depending on stress level and duration of exposure, and the complex nature of plant response to tolerate cold stress, visual damage to seedlings exposed to low-temperature stress was assessed. The major QTL on chromosome 12, associated with tolerance to wilting and necrosis, was particularly interesting and it may be useful as a target for varietal improvement and positional cloning. In the field, adequate cold tolerance at the seedling stage may allow early sowing, because cold-tolerant seedlings should be able to survive and develop normally, thereby ensuring uniform crop establishment. Since the QTLs here were identified from growth-chamber studies under severe-stress levels, the usefulness of these QTLs should, therefore, be evaluated under field conditions.
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Acknowledgements |
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We are grateful to Cynthia Andaya for critically reading the manuscript, to Mike Saltveit, Abdel Ismail and KK Jena for valuable suggestions, to the Rockefeller Foundation for the fellowship awarded to VC Andaya, and to the California Rice Research Board for the partial support on this study.
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References |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Allen DJ, Ort DR. 2001. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science 6, 36–42.[CrossRef][Web of Science][Medline]
Andaya VC, Mackill DJ. 2003. QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonicaxindica cross. Theoretical and Applied Genetics 106, 1084–1090.[Web of Science][Medline]
Bertin P, Kinet JM, Bouharmont J. 1996. Evaluation of chilling sensitivity in different rice varieties. Relationship between screening procedures applied during germination and vegetative growth. Euphytica 89, 201–210.[CrossRef]
Gesch RW, Heilman JL. 1999. Responses of photosynthesis and phosphorylation of the light-harvesting complex of photosystem II to chilling temperature in ecologically divergent cultivars of rice. Environmental and Experimental Botany 41, 257–266.
Glaszmann JC. 1987. Isozymes and classification of Asian rice varieties. Theoretical and Applied Genetics 74, 21–30.[CrossRef]
Glaszmann JC, Kaw RN, Khush GS. 1990. Genetic divergence among cold tolerant rices (Oryza sativa L.). Euphytica 45, 95–104.[CrossRef]
Haley CS, Knott SA. 1992. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69, 315–324.[Web of Science][Medline]
IRRI. 1988. Standard evaluation system for rice. International Rice Research Institute, Los Baños, Philippines.
Jansen RC, Stam P. 1994. High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136, 1447–1455.[Abstract]
Kaneda C, Beachell HM. 1974. Response of indica–japonica rice hybrids to low temperatures. SABRAO Journal 6, 17–32.
Kim KM, Sohn JK, Chung IK. 2000. Analysis of OPT8(511) RAPD fragments closely linked with cold sensitivity at seedling stage in rice (Oryza sativa L.). Molecules and Cells 10, 382–385.[Web of Science][Medline]
Kwak TS, Vergara BS, Nanda JS, Coffman WR. 1984. Inheritance of seedling cold tolerance in rice. SABRAO Journal 16, 83–86.
Lander ES, Green P, Abrahamson J, Barlow A, Daly M, Lincoln SE, Newburg L. 1987. Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181.[CrossRef][Medline]
Lee TM, Lur HS, Chu C. 1993. Role of abscisic acid in chilling tolerance of rice (Oryza sativa L) seedlings.1. Endogenous abscisic acid levels. Plant, Cell and Environment 16, 481–490.[CrossRef]
Lee TM, Lur HS, Chu C. 1995. Abscisic acid and putrescine accumulation in chilling-tolerant rice cultivars. Crop Science 35, 502–508.
Mackill DJ. 1995. Classifying japonica rice cultivars with RAPD markers. Crop Science 35, 889–894.
McCouch SR, Teytelman L, Xu Y, et al. 2002. Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Research 9, 199–207.[Abstract]
Misawa S, Mori N, Takumi S, Yoshida S, Nakamura C. 2000. Mapping of QTLs for low-temperature response in seedlings of rice (Oryza sativa L.). Cereal Research Communications 28, 33–40.
Nagamine T. 1991. Genic control of tolerance to chilling injury at seedling stage in rice. Japanese Journal of Breeding 41, 35–40.
Nakagahra M, Okuno K, Vaughan D. 1997. Rice genetic resources: history, conservation, investigative characterization and use in Japan. Plant Molecular Biology 35, 69–77.[CrossRef][Web of Science][Medline]
Ni J, Colowit PM, Oster JJ, Xu K, Mackill DJ. 2001. Molecular markers linked to stem rot resistance in rice. Theoretical and Applied Genetics 102, 511–516.[CrossRef]
Oka HI. 1988. Origin of cultivated rice. Tokyo: Elsevier.
Peterson ML, Lin SS, Jones D, Rutger JN. 1974. Cool night temperatures cause sterility in rice. California Agriculture 28, 12–14.
Redoña ED, Mackill DJ. 1996. Genetic variation for seedling vigour traits in rice. Crop Science 36, 285–290.
Saltveit ME. 2001. Chilling injury is reduced in cucumber and rice seedlings and in tomato pericarp discs by heat-shocks applied after chilling. Postharvest Biology and Technology 21, 169–177.[CrossRef]
Saruyama H, Tanida M. 1995. Effect of chilling on activated oxygen-scavenging enzymes in low-temperature-sensitive and -tolerant cultivars of rice (Oryza sativa L.). Plant Science 109, 105–113.[CrossRef]
Sonoike K. 1998. Various aspects of inhibition of photosynthesis under light/chilling stress: ‘Photoinhibition at chilling temperatures’ versus ‘Chilling damage in the light’. Journal of Plant Research 111, 121–129.
Sthapit BR, Witcombe JR. 1998. Inheritance of tolerance to chilling stress in rice during germination and plumule greening. Crop Science 38, 660–665.
Sthapit BR, Witcombe JR, Wilson JM. 1995. Methods of selection for chilling tolerance in Nepalese rice by chlorophyll fluorescence analysis. Crop Science 35, 90–94.
Utz HF, Melchinger AE. 1996. PLABQTL: A program for composite interval mapping of QTL. 2 (http://probe.nalusda. gov:8000/otherdocs/jqtl/jqtl1996–01/utz.html).
Yoshida H, Kato A. 1994. Cold-induced accumulation of RNAs and cloning of cDNAs related to chilling injury in rice. Breeding Science 44, 361–365.
Zeng ZB. 1994. Precision mapping of quantitative trait loci. Genetics 136, 1457–1468.[Abstract]
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