Crop Science 43:508-510 (2003)
© 2003 Crop Science Society of America
CROP BREEDING, GENETICS & CYTOLOGY
Inheritance of Apetalous Flowers in a Mutant of Oilseed Rape
Lixi Jianga and
Heiko C. Becker*,b
a Inst. of Crop Sci., Zhejiang Academy of Agric. Sci., New Shiqiao Road 198, Hangzhou 310021, PR China
b Inst. of Agron. and Plant Breeding, Georg-August-Univ. Göttingen, Von Siebold Straße 8, 37075 Göttingen, Germany
* Corresponding author (hbecker1{at}gwdg.de)
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ABSTRACT
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Oilseed rape (Brassica napus L.) genotypes with reduced petal size are thought to have advantages in photosynthetic capacity and in disease resistance. This study was conducted to analyze the inheritance of a completely apetalous mutant that was induced by mutagenic treatment. The mutant ap-Tengbe was crossed with the German winter rapeseed cultivar Falcon. The F1, the F2, and both backcrosses including reciprocal generations were grown in field experiments at Göttingen, Germany, in 1997-1998 and at Hangzhou, China, in 1998-1999. The apetalous character of ap-Tengbe is regulated by an interaction of cytoplasmic genes and two pairs of nuclear genes. Completely apetalous flowers are only expressed in genotypes with the ap cytoplasm and two homozygous recessive genes. In conclusion, the mutant ap-Tengbe is useful to produce completely apetalous genotypes, but cytoplasmic effects have to be considered.
Abbreviations: CMS, cytoplasmic male sterility • EMS, ethyl methane sulfonate • PDgr, petalous degree
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INTRODUCTION
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ONE OF THE characteristics of the family Brassicaceae is its typical flower with four free petals. In Brassica species, mutants have been observed which show increased petals, reduced petals, or complete absence of petals (apetalous) (Singh, 1961a,b; Cours and Williams, 1977; Buzza, 1983; Lü and Fu, 1990; Fray et al., 1997). Apetalous genotypes may be more efficient in photosynthesis and reallocation of assimilates because the yellow petal layer of Brassica oilseed crops reflects a large part of the photosynthetically active radiation (Chapman et al., 1984; Yates and Steven, 1987; Mendham et al., 1991; Fray et al., 1996; Jiang and Becker, 2001a). Moreover, apetalous types may avoid some diseases, especially stem rot caused by Sclerotinia sclerotiorum (Lib.) de Barry and downy mildew caused by Peronospora parasitica (Pers.:Fr.) (McLean, 1958; Krüger, 1975; Kapoor et al., 1983). On young petals, ascospore adhesion, germination, penetration of the host, and collapse of epidermal cells were observed by scanning electron microscopy. Mycelia on petals invade leaf tissues and then infect plants. In contrast, ascospores landing directly on leaf surfaces do not germinate (Jamaux et al., 1995).
Apetalous genotypes in Brassica species have different genetic origins. Most of them were either discovered as spontaneous mutations (Singh, 1961a,b; Buzza, 1983; Lü and Fu, 1990), or were by-products of other research (Malik et al., 1999). The inheritance of the apetalous character is different for different sources. In B. rapa, the trait is controlled by one single recessive gene (Singh, 1961a,b; Cours and Williams, 1977). Genotypes with apetalous flowers have been most thoroughly investigated in B. napus. Depending on the source of the apetalous character, the trait is controlled by two recessive genes (Buzza, 1983), four recessive genes (Lü and Fu, 1990), an epistatic interaction between recessive alleles at a pair of homologous loci, or interaction between alleles at three loci (Kelly et al., 1995). The objective of this study was to investigate the inheritance of apetalous flowers in ap-Tengbe, which was identified in European winter oilseed rape after mutagenic treatment of seeds with ethyl methane sulfonate (EMS).
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MATERIALS AND METHODS
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The apetalous mutant ap-Tengbe was observed after several mutagenic seed treatments with EMS (Tengbe, 1990). At the beginning of this program, the B. napus spring rapeseed cultivar Oro was treated twice and genotypes with low linolenic acid content were selected (Rakow, 1973; Röbbelen and Nitsch, 1975). One line (M48) was crossed with winter rapeseed, backcrossed two times to several adapted winter rapeseed cultivars, and selected for agronomic performance until F4. Nine F4 lines were again treated with EMS and 3096 M1 plants were grown as a bulk. In the M2 generation, a total of 17 899 plants were grown in the field. One of these plants was apetalous. This plant was selfed for six generations with selection for stable expression of the apetalous type. This mutant ap-Tengbe has completely apetalous flowers.
To produce the material for the present study, the German winter rapeseed cultivar Falcon was crossed with the mutant ap-Tengbe and the following generations including reciprocals were produced (female parent is listed first): F1, Falcon x ap-Tengbe; R-F1, ap-Tengbe x Falcon; BC11, F1 x ap-Tengbe; R-BC11, ap-Tengbe x F1; BC12, F1 x Falcon; R-BC12, Falcon x F1; F2, selfing (Falcon x ap-Tengbe); R-F2, selfing (ap-Tengbe x Falcon).
All generations except the R-F2 were field grown at two very diverse environments: under the temperate climate at the Experimental Farm of the University Göttingen at Reinshof in Northern Germany in 1997-1998 and under subtropical conditions at the Experimental Farm of Zhejiang Academy of Agricultural Sciences at Hangzhou in Southeast China in 1998-1999. The R-F2 population was observed only at Hangzhou. Normal local agronomic practices were used at both sites. During flowering season, 20 April to 25 May in Göttingen or 1 April to 5 May in Hangzhou, the mean precipitations were 
50 and 94 mm, the average temperatures were 10.4 and 13.7°C and the mean daily sunshine was 5.2 and 4.7 h for Göttingen and Hangzhou, respectively.
Petalous degree (PDgr) was calculated according to Buzza (1983):
with Pi = the number of petals on the ith flower and N = total number of the flowers counted. At least 25 open flowers of each plant were counted for number of petals at the early flowering stage. Curled and wilted petals less than one-fourth of the length of the normal petals were not counted as a petal. Plants with PDgr <10, 10 to 90, and >90 were classified into the groups of apetalous, partially apetalous, and normal-petaled genotypes, respectively. The fit of theoretically expected and observed segregation ratios was tested by Chi-Square test (
2).
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RESULTS AND DISCUSSION
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Despite large environmental differences in average temperature, rainfall, and daily sunshine during the flowering season, the results from the two locations agreed very well with each other. At both locations, BC11, R-BC11, F2, and R-F2 generations segregated for PDgr (Table 1), while all plants in F1, R-F1, BC12, and R-BC12 had normal petals. At both Göttingen and Hangzhou, approximately one-fourth of the plants in BC11 were partially apetalous and the others had normal petals. In the F2 generation, about one-sixteenth of the plants were partially apetalous and the others were normally petaled. No completely apetalous plants were found in BC11 and F2 populations, but they were observed in the reciprocal generations. At both sites, the segregation for apetalous, partially apetalous, and normally petaled plants showed a 1:2:1 ratio in the R-BC11, and the observed segregation in R-F2 at Hangzhou was 10 apetalous, 64 intermediate, and 128 normally petaled plants.
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Table 1. Distribution for petalous degree (PDgr) at Göttingen, Germany, 1997-1998 (GOE) and Hangzhou, China, 1998-1999 (HAN).
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To explain these results, we conclude that the apetalous character in ap-Tengbe is regulated by interaction of cytoplasmic genes and two nuclear genes. The apetalous character is only expressed completely if plants are homozygous for two recessive genes and if they have a cytoplasm supporting expression of apetalous flowers (Table 2). The parent Falcon with normal petals has the normal cytoplasm (CN) and four alleles at two nuclear genes coding for normal petals (P1P1P2P2), whereas the apetalous ap-Tangbe mutant has the apetalous cytoplasm (Cap) and four alleles coding for the absence of petals (p1p1p2p2). Alleles for petals are dominant to those for apetalous flowers. The F1 plants (Falcon x ap-Tengbe) have CN and the nuclear genes P1p1P2p2, and express normal petals. The R-F1 plants (ap-Tengbe x Falcon) have the cytoplasm for apetalous flowers, Cap, but they still show normal petals due to dominant effects of both P1 and P2 alleles. For the same reason, all plants in the BC12 and the R-BC12 have normal petals. In BC11 and F2, all plants have the normal cytoplasm CN, and only genotypes with p1p1p2p2 are partially apetalous and the genotypes with three or less recessive alleles of p1 and p2 have normal petals. Therefore, the expected segregation in BC11 and F2 populations is 0:1:3 and 0:1:15, respectively, for apetalous, partially apetalous, and normally petaled plants. However, the R-BC11 and R-F2 plants with Cap cytoplasm show a segregation of 1:2:1 or 1:6:9 for apetalous, partially apetalous, and normally petaled types, respectively. Chi-square tests (2) show that all observed segregation ratios agree with theoretical expectations (Table 3).
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Table 2. Genetic interpretation of apetalous, partially apetalous, and normally petaled phenotypes of oilseed rape.
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Table 3. Chi-Square test (2) for segregation of petalous degree (PDgr) in segregating populations of oilseed rape grown at Göttingen, Germany, 1997-1998 (GOE) or Hangzhou, China, 1998-1999 (HAN).
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The genetic analysis of the apetalous character in the ap-Tengbe mutant was based on the rating scale proposed by Buzza (1983). However, the definition of PDgr in this study is different from Buzza's (1983), who defined as partially apetalous intermediate type a PDgr between 10 and 80%, instead of 10 and 90% as was done here. According to our field observation, even with PDgr of 80 to 85%, some completely apetalous flowers occurred at times on an inflorescence; whereas with a PDgr of >90%, completely apetalous flowers were extremely rare.
The genetic interpretation of our results is not absolutely conclusive for one of the generations, the reciprocal R-F2 (ap-Tengbe x Falcon), where two alternative explanations are possible. The observed segregation ratio in R-F2 was 10:64:128 for apetalous, partially apetalous, and normally petaled types (Table 1). The theoretical segregation of 1:6:9 is based on the assumption that the genes are acting independently and additively. If, however, the gene for normal petals would act epistatically over the apetalous gene in the genotypes Cap(P1P1p2p2) or Cap(p1p1P2P2), the theoretical segregation in R-F2 should be 1:5:10 for apetalous, partially apetalous, and normally petaled phenotypes. According to Chi-square tests, both hypotheses are possible; however, the later hypothesis fits better to the observed ratio (2 = 0.49 for N0).
The inheritance of apetalous flowers in ap-Tengbe resembles that of cytoplasmic male sterility (CMS) in the way the cytoplasm interacts with nuclear genes in determining phenotypes (Yang and Fu, 1990; Stiewe and Röbbelen, 1994; Delourme and Budar, 1999). It was recognized that CMS is often linked with small petals or a reduced petal number (Shiga, 1980; McVetty et al., 1989). We observed a reduced pollen production in the apetalous ap-Tengbe mutant; however, the apetalous types have normal seed set after selfing. Cytoplasmic effects on the inheritance of the apetalous character have not been reported before, although Buzza (1983) and Lü and Fu (1990) studied possible cytoplasmic effects. They made crosses between their apetalous phenotypes and normally petaled parents and compared the reciprocal F1 and F2 populations without observing significant cytoplasmic effects. In all other studies on the inheritance of the apetalous trait, the potential for cytoplasmic effects was not considered.
In conclusion, the ap-Tengbe mutant can be successfully used to develop completely apetalous breeding lines of B. napus oilseed rape, but cytoplasmic effects have to be considered. Young plants show some chlorophyll deficiency and pollen production is reduced. Ap-Tengbe has been agronomically improved by crossing with the cultivar Falcon and subsequent selection. Apetalous lines with ap-Tengbe background showed clearly larger leaf area index and heavier dry matter biomass in comparison to sister lines with normal flower petals, particularly under conditions of more dense plant population and higher N application (Jiang and Becker, 2001a).
The expression of the apetalous character was environmentally stable at the two very different locations. However, PDgr was always recorded at the beginning of flowering, and at the end of the flowering period even apetalous genotypes sometimes develop some petals. The influence of external and internal factors during the flowering period on the expression of the apetalous phenotype has been described in detail in a separate publication (Jiang and Becker 2001b).
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ACKNOWLEDGMENTS
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The authors thank Prof. Dr. G. Röbbelen and Dr. D. Stelling for developing and providing the ‘ap-Tengbe’ material, and Mrs. D. Zhang for assisting in sowing and field observation at Hangzhou. The first author was financially supported by the German Academic Exchange Services (DAAD).
Received for publication February 11, 2002.
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REFERENCES
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ABSTRACT
INTRODUCTION
