Elucidating the genetic control of heritable traits of plants is vital for improvement. The inheritance of flower shapes has been investigated in various ornamental plant species, e.g., the recessive allele was responsible for the single flower phenotype in carnation (Yagi et al. 2014) and Petunia hybrida (Liu et al. 2016). In contrast, the double-flower phenotype is a single recessive trait in gentians (Tasaki et al. 2017) and peach (Meng et al. 2019). For chrysanthemums, research on the inheritance mode of flower shape has progressed rather slowly, probably attributing to its nature of genome complexity and high heterozygosity (Anderson and Ascher 2000; Tang et al. 2009; Zhang et al. 2011; Su et al. 2016). Furthermore, several papers have attempted to uncover the genetic law. Dejong and Drennan (1984) reported that singleness was partially dominant to doubleness. Similarly, Lim et al. (2014) suggested an incomplete dominance for double and single flowers in the 'Falcao' × 'Frill Green' population. Zhu et al. (2012) reported that the hybrids differentiated obviously from their parents and represented three flower types, including standard anemone type, mid-anemone type, and non-anemone type, and most were anemone type in a backcross population. The current work found that the anemone flower shapes in hybrids were not entirely segregated, accompanied by the generation of intermediate types. In most crosses of contrasting flower type parents, anemone and nonanemone types were segregated into a 1:3 ratio, suggesting the dominance of nonanemone type over anemone type. Comparatively, the anemone and nonanemone segregation ratio in the two crosses Co5 and Bco5, derived from parents 'XF' and 'QX096' also with contrasting flower types, deviated from the above separation ratio, but following 1:1 and 3:1 ratios, respectively. It is noteworthy that the anemone × anemone crosses also generated nonanemone-type flowers, with an anemone to nonanemone segregation ratio of 3:1. Therefore, the current research suggested that the inheritance of anemone flower shape is far more complex than expected and might be associated with more than one gene or be modified by different genes. The findings may reflect, to some extent, the complex genetic effects identified for the tubular floral traits relevant to anemone type in our recent research (Yang et al. 2019b).
Maternal inheritance is the non-Mendelian transmission of traits from mothers to their offspring (Lande and Kirkpatrick 1990). It has important implications for evolution in natural populations and practical applications in the economic improvement of species (Chandnani et al. 2017). In chrysanthemum, maternal inheritance has been proposed for flat-and spoon-type ray floret (Xu et al. 2000) and red color (Chen et al. 2003). In the current research, an important goal was to dissect the effect of maternal inheritance on anemone-type chrysanthemum. From the crosses derived from the same male anemone type parent and different female parents (Co1, Co2, Co3, and Co4) or from the same female anemone type parent and the different male parent (Co4, Co5, and Co6), we could observe a maternal or paternal effect on the inheritance of anemone type flower. To further insight into the parent effect, we produced three sets of reciprocal crosses (Co3 vs. Bco3, Co4 vs. Bco4, and Co5 vs. Bco5) with contrasting. In the light of the similar segregation in the reciprocal crosses, say Co3 vs. Bco3 and Co4 vs. Bco4 derived from contrasting parents, however, it seems difficult to decide on the maternal or paternal inheritance mode for anemone flower shape. Therefore, we cannot conclude the inheritance mode of anemone-type flower due to the segregation complexities in the current work. To our expectation, crosses Co5 vs. Bco5 derived from both anemone type parents generated more anemone type progenies, casting light on the future breeding success of anemone-type chrysanthemums. In other words, it would be fruitful to develop desirable anemone-type varieties by crossing anemone-type parents.
The hybrids' performance displayed extensive transgressive segregation and significant heterosis in chrysanthemum (Zhang et al. 2011; Yang et al. 2015; Su et al. 2017). However, most floral traits in the current crosses showed some extended decline and exhibited a negative MPH value. This contradiction may be due to the differences in species, materials, morphological characteristics, or environmental factors involved in the above studies. Moreover, high CV values were observed in the F1 populations, indicating significant potential for selecting elite hybrids with desirable flower types. Estimating the genetic distance between parents is entirely meaningful for predicting heterosis. The morphological traits-derived genetic distance is widely applied for the advantage of being convenient and straightforward (Espósito et al. 2014). The phenotypic parent-wise genetic distance (PD) was significantly and negatively correlated with MPH for LLL, TFL, TFW, and TFL/SL in our study. However, PD and mean values of hybrid progenies were not significantly correlated for all investigated floral traits (Table 4). These findings are in accordance with Riday et al. (2003) and Geleta et al. (2004), who found that PD showed a significant correlation with tested agronomic traits in Medicago stiva and pepper. Nevertheless, Wegary et al. (2013) observed that non-significant correlation between PD and heterosis in maize. Hence, our results suggested the possibility of predicting the heterosis of floral traits by PD.
Previous research has proposed that, molecular markers could improve the heterosis prediction efficiency (Buti et al. 2013; Frisch et al. 2010; Sang et al. 2015). Huang et al. (2015) and Tian et al. (2017) proposed that selecting favoring loci from molecular makers would effectively facilitate the prediction of heterosis. In chrysanthemum, Su et al. (2016) found that the genetic distance estimated by the QTL-linked markers could better predict heterosis of waterlogging tolerance traits. In our case, the SNPs-based parent-wise geneic distance did not significantly correlate with heterosis in the current study. Thus, it did not satisfactorily predict heterosis and average phenotypic values concerning flower type traits. Weak correlations were also reported in crops including maize (Devi and Singh 2010; Ndhlela et al. 2015), rapeseed (Brassica napus L.) (Tian et al. 2017) and wheat (Chen et al. 2010), and pepper (Geleta et al. 2004). The low level of correlation could result from several reasons, such as a lack of corresponding genetic marker associated with genes controlling the target traits and unequal genome coverage, which would contribute to F1 performance and heterosis. Otherwise, it may also result from an extensive genetic differentiation among inter-specific hybridization progenies and genetic × environmental interactions (Ndhlela et al. 2015). In future, implementing DNA markers associated with genes responsible for the characteristics of interest, combined with the combining ability analysis, may be a promising approach for heterosis prediction in chrysanthemum.
In conclusion, the present study represented a worthwhile attempt to assess the inheritance pattern of anemone flower shape, its related tubular floral traits, and the prediction of heterosis. The majority of the assayed floral traits exhibited considerable variation, underlying the potential for future improvement of desirable chrysanthemums. The hybrids' performance involved less influence of maternal or paternal effects but related to a specific parental cultivar. The morphology other than the genome-wide SNP-based parent-wise genetic distance is promising in predicting the heterosis. The outcome of this study help understand the inheritance of flower type in chrysanthemums and lays a foundation for parental selection and genetic improvements of desired traits.
Author contribution statement FZ conceived and designed the project, FC, WF, and ZG provided the materials, XY, JS, and YQ conducted experiments, XY and FZ analyzed the data and wrote the manuscript. All authors read and agreed to the submitted version of the manuscript.