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. 2022 Feb 26;34(7):2455–2461. doi: 10.1093/plcell/koac070

Mendelian and non-Mendelian genetics in model plants

Ortrun Mittelsten Scheid 1,✉
PMCID: PMC9252483  PMID: 35218351

Abstract

The “Mendelian Rules” of inheritance are cornerstones of genetics, described in Mendel’s seminal publication from 1866. The experimental results and their interpretation have been discussed in numerous ways. This perspective emphasizes the contribution of Mendel’s preparations prior to his crossing experiments to the discovery of Mendelian genetics. This thoughtful experimental design, and some fortune, avoided pitfalls that could have resulted in non-Mendelian inheritance.

Introduction

Gregor Mendel performed carefully controlled crossing experiments, mainly with pea plants, and discovered regularity and predictability of parental traits as well as new traits in the progeny, describing the principles of uniformity, segregation, and independent combination of traits. His work is a great example of how plants as experimental model organisms can contribute to ground-breaking discoveries. The meticulous preparation and design of Mendel’s experiments were a prerequisite to obtaining clear and reproducible results, and this deserves as much respect as their thoughtful interpretation.

Despite their applicability in other organisms beyond pea seeds and plants, there are numerous examples in which inheritance does not follow Mendelian rules. Shortly after the significance of Mendel’s work was finally recognized by a larger scientific community, evidence was reported, intriguingly also with pea plants, that were inconsistent with the Mendelian rules (Bateson and Pellew, 1915). This case is now interpreted as paramutation, an epigenetic phenomenon apparently violating the expectation of independent segregation. We now know of many other examples that violate Mendelian expectations. While epigenetic determinants are responsible for some, other cases of non-Mendelian inheritance have simple genetic explanations.

For several reasons, Zea mays, Arabidopsis thaliana, and other plants have replaced Pisum sativum as models for genetic research. However, research in genetics and breeding are based on Mendel’s contributions to our understanding of inheritance. Mendel as name patron for a plant science institute in Austria gives credit to that. The 200th anniversary of Johann Gregor Mendel’s birthday in 2022 is a timely occasion to honor this great scientist in this journal and to provide a brief perspective on our understanding of Mendelian and non-Mendelian modes of inheritance.

Formulation and fortune

The main scientific work of Johann Gregor Mendel was published in 1866 in an article entitled “Versuche über Pflanzenhybride” (experiments about plant hybrids) in the proceedings of a local naturalist association (Mendel, 1866). It was translated into English by William Bateson in 1902 (Berger, 2022); an English version is available at http://bshs.org.uk/bshs-translations/mendel/2016.

In the introductory remarks, Mendel explains the rationale for his experiments: he refers to previous researchers that had generated hybrids by artificial fertilization and observed striking regularity between hybrids from the same combination of parents. However, he points to the lack of “a generally valid law for the formation and development of hybrids” and lists the shortcomings and difficulties to address them. His success to master what he saw as a “far-reaching task that takes quite some courage to undertake but appears to be the only correct way” is a milestone in the history of genetics, but it was decades before the relevance of this report was recognized by a wider scientific community (Wilkie, 1962). Soon after, geneticists and statisticians debated if the results presented by Mendel were “too good to be true” (Fisher, 1936; Franklin et al., 2008), although they have been reproduced in numerous experiments with a vast range of different organisms ever since. A recent comprehensive re-examination of Mendel’s segregation ratios does not support the notion that they differ from expectation (Ellis et al., 2019), allowing us to consider this debate closed.

While the data in Mendel’s main publication received extensive attention (if belatedly), the introductory part of his monograph was much less discussed. But it is worth a closer look as it illustrates his appreciation of the importance of careful experimental design to the success of his experiments. Mendel argued for the choice of the garden pea as his main test plant because the shape of the flowers would allow easy removal of the immature anthers (emasculation) and protect against unwanted cross-pollination. Further advantages that he listed included the relatively short life cycle of the plants, easy cultivation in a greenhouse or garden, as well as the natural variation provided by breeders. In addition, Mendel considered that high fertility, complete collection of all progeny individuals, and avoidance of loss by pathogens would be essential for the research. He also recognized that the crosses should be made in reciprocal directions, using each line alternatively as male or female parent. For fully 2 years before carrying out his most important crosses, Mendel studied 34 varieties of garden peas under his culture conditions, to observe stability and uniformity of the traits. Among 22 selected varieties, he observed and documented 15 parameters. He distinguished features with digital inheritance (either–or) from those with quantitative differences (more or less). He excluded the latter from further experiments and settled on plants that differed in seven digital traits for his crosses, that is to produce the plant hybrids. Among the selected traits were features of flowers and pods, and of course the famous color and shape variants of the seeds that are used to illustrate the Mendelian rules in most textbooks (Figure 1). The focus on the seed phenotype had the additional benefit that the phenotype of the progeny could be scored immediately, reducing time, space, and labor to generate the data. This extensive and careful planning (Mendel, 1866) contributed to the clear results of the experiments and allowed him to recognize discrete segregation patterns. Notwithstanding, and because many factors can lead to non-Mendelian inheritance as described later, Mendel had some fortune on his side that helped to avoid circumstances under which the data would have been less easy to interpret, despite all prudence.

Figure 1.

Figure 1

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Pisum sativum as model plant in genetics. Left: Pea seeds differing in color (green or yellow) and shape (smooth or wrinkled), as used in Mendel’s crosses. Right: Historical school teaching material. The chart demonstrates the uniformity of the phenotype in the F1 generation, and the segregation and appearance of new combinations alongside the parental phenotypes in the F2 generation. Figures reproduced from (Mittelsten Scheid, 2017).

Peas and paramutation

Among several scientists that “rediscovered” and confirmed Mendel’s findings in the early 20th century was the British biologist William Bateson, who introduced the term “genetics” to study inheritance. He and his co-worker Caroline Pellew performed many experiments with pea plants. It is an oddity in science history that among their crosses were some for which inheritance seemingly did not follow the Mendelian rules of independent segregation. If plants with the “rogue” phenotype (a morphological aberration of leaves and stems, Figure 2) were used as a parent, the regular morphology was not recovered by segregation as expected by the Mendelian rules of segregation (Bateson and Pellew, 1915). This is now acknowledged as the first case of paramutation (Chandler and Stam, 2004) described below. The pea example of paramutation is hardly studied on the molecular level, but there is evidence that the mutant rogue phenotype is correlated with differential DNA methylation patterns, indicating epigenetic differences, at several loci (Santo et al., 2017; Pereira and Leitão, 2021).

Figure 2.

Figure 2

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Pea plant branches differing in morphology: the regular (left) and the “rogue” phenotype characterized by narrower, pointed leaves, and stipules (right). John Innes Archive courtesy of the John Innes Foundation.

In the early 20th century, geneticists had chosen plants other than peas as experimental models for crossing experiments but used criteria similar to those that Mendel developed when he selected peas to investigate inheritance. For example, maize is an important crop plant in the Americas with many attributes that made it amenable for genetic analysis: male and female organs are separate, unwanted cross pollination can easily be avoided, and reciprocal crosses are easy to carry out. Each cross provides high seed numbers, and the attachment of the kernels on the cob allows estimation of fertility resulting from crosses. Probably most important was the availability of kernel color variants which were easy to score in situ on the ear in the F1 progeny. While most of the kernel mutant variants were inherited according to Mendelian rules of independent segregation, there were crosses that resulted in deviations from the expected ratios. One such set of crosses was followed up by Alexander Brink. He observed that the weakly expressed Rst allele of the kernel color-determining locus r1 appeared dominant in combination with a strongly expressed Rr allele in the F1 generation: all F1 plants developed the color characteristic of the Rst allele. Furthermore, no plants in the F2 generation expressed the strong allele even though the chromosome that carried this previously active allele was present. It was as though the weakly expressed Rst allele had weakened the strong expressing Rr allele. Furthermore, the newly weakened allele remained weak in subsequent generations and could weaken another strong allele upon backcrossing. Because it appeared as if the Rr allele had been mutated, in a directed, non-random way, and could mutate other alleles, Brink called this process paramutation (Brink, 1958; Brink et al., 1968). This term turned out more succinct than “somatic conversion,” used to describe similar phenomena observed for the sulfurea gene in tomato (Hagemann, 1958; Hagemann and Snoad, 1971). Other maize loci such as b1, pl1, and p1 (Coe, 1959; Hollick et al., 1995; Sidorenko and Peterson, 2001) were also reported to be susceptible to paramutation. Although different in detail, and likely including the case of the “rogue” peas, they have in common that gene expression of one allele is reduced and the original allele is not expressed as it was in the parental line, in contrast to the expectation based on Mendelian inheritance. This, and the potential for secondary paramutation, can have a large impact on allele distribution in a population, and it is not restricted to plants (reviewed in Hollick, 2017).

The molecular basis of paramutation at a number of maize loci is relatively well understood and includes several features, like sequence and structure of the alleles, interaction between enhancer and promoter regions, differential DNA methylation and chromatin organization, transcription rates, transcript types and small RNA molecules, and the requirement for many well-characterized epigenetic regulators of the RNA-directed DNA methylation pathway (for review see Hollick, 2017). However, only a small subset of epigenetically modified alleles participates in paramutation. Nevertheless, many cases of paramutation may have gone undetected, as they may affect inheritance of traits less easily scorable than pigmentation, or they could already have modified all alleles in a population in the past. Paramutation is strong evidence in support of the hypothesis that acquired epigenetic changes may be stably inherited, determine plant phenotypes in progeny, and as such, represents one variant of non-Mendelian genetics. It should be emphasized that this is not the case for other acquired epigenetic changes, exemplified by the process of vernalization, a memory of a cold period that must precede flowering in some plants, which is reset between generations (Crevillén et al., 2014). Thus, epigenetic states exhibit a wide range of permanency: minimal in case of regular resetting, moderate in parental or grandparental effects relevant only for a few generations, or maximum in paramutation-like cases that represent true transgenerationally stable changes.

Circumventing conundrums

Epigenetically encoded regulation of gene activity is one—and likely a frequent—source of non-Mendelian inheritance, but there are several exclusively genetic reasons why traits are seemingly or indeed inherited in a way that is not compatible with the Mendelian rules. These include linkage disequilibrium, polygenic traits, polyploidy, aneuploidy, heterosomes, B chromosomes, meiotic drive, cytoplasmic inheritance, agamospermy, and imprinting. These phenomena that can cause non-Mendelian inheritance and are relevant in plant genetics are described in the following paragraphs.

Linkage disequilibrium and polygenic traits

Genetic information is organized on different chromosomes of different length, resulting in genetic linkage of genes. There are seven chromosomes in P. sativum, and two and three of the genes encoding Mendel’s traits are located on the chromosome 1 or 4, respectively (Ellis et al., 2011). In hindsight, it is surprising that most trait combinations delivered results like unlinked genes, but this is explained by the large size of the pea chromosomes and the distance of the loci, allowing high recombination frequency and de facto no linkage disequilibrium (Blixt, 1975; Reid and Ross, 2011). Any closer linkage would have blurred the data for some crossing combinations, preventing the observation of new combinations and their interpretation as the result of independent segregation. Similarly, it was fortunate that the pea seed traits were monogenic, determined by single genes (Reid and Ross, 2011; Ellis et al., 2019; Berger, 2022), which upon mutation caused traits that had been of interest to farmers. Mendel depended on the material available at his time, but his careful characterization of the material prior to the crosses avoided the pitfall of polygenic traits determined by several genes.

Polyploidy

Another lucky strike with the choice of P. sativum was its diploid karyotype, as it has two copies of each chromosome. Most angiosperms, and especially many crop plants, have more than two chromosomes of the same type (Masterson, 1994), referred to as polyploidy. In autotetraploid species, with four chromosome sets from the same species, like potato, independent segregation of a recessive trait would mean that the trait would be expressed in only 1 out of 36 F2 plants (Comai, 2005). In autohexaploid plants with six copies of each chromosome, the frequency of a recessive trait in the F2 could be further reduced to 1 in 64. In addition, autopolyploid karyotypes have the potential for double reduction, in which distal regions from two sister chromatids can be included in the same gamete. This exceptional configuration occurs if two recombined chromosomes move to the same pole in anaphase I, a situation excluded in diploids (Levings and Alexander, 1966). This can result in a complexity of segregation data that could be disentangled only once the concept of meiotic chromosome recombination was understood.

Aneuploidy, heterosomes, and B chromosomes

While multiplication of the entire chromosome complement makes chromosome recombination and separation in meiosis more complex than in diploids (reviewed in Zielinski and Mittelsten Scheid, 2012), it still allows calculating expected segregation ratios if the combinatorial parameters are known. In contrast, in case of imbalanced numbers of individual chromosomes characteristic of aneuploids, this is impossible due to their random segregation during meiosis, leading to distorted segregation. This might result in modified trait expression: many examples demonstrate that different conditions of aneuploidy have substantial influence on plant phenotypes (for review, Birchler and Veitia, 2021). Important traits can also be encoded on specialized “extra” chromosomes which are asymmetrically distributed during meiosis: many dioecious plants have heterosomes, sex chromosomes that determine the formation of only male or female organs in the flowers. While this is less frequent than polyploid karyotypes in angiosperms, progress in genome sequencing revealed that sex chromosomes determine multiple phenotypically relevant traits in addition to flower type (Carey et al., 2021). This could be true also for so-called B chromosomes that occur in addition to the set of autosomes (A chromosomes), in varying numbers, types, and stability upon transmission in different species (reviewed by Banaei-Moghaddam et al., 2015; Ahmad and Martins, 2019). How much B chromosomes contribute to trait formation has just begun to be investigated, but like heterosomes, their asymmetric segregation results in irregular segregation patterns. Besides differences in B chromosome numbers between individual plants, B chromosomes can undergo a programmed elimination during development of an individual plant, concurrent with massive gene expression changes, including that of genes on the B chromosomes themselves (Boudichevskaia et al., 2020). There are neither sex chromosomes nor B chromosomes in P. sativum but some crosses have resulted in trisomic pea plants with three rather than the regular two copies of individual chromosomes, resulting in characteristic phenotypes (Berdnikov et al., 2003). Hugo de Vries, one of the geneticists that recognized the relevance of Mendel’s work around 1900, hypothesized that the frequent intergenerational morphological variation in the evening primrose Oenothera lamarckiana would indicate the formation of new species by mutations, but the variation was later found to be linked to extra chromosomes and dosage imbalance, not to polymorphisms in DNA sequence (reviewed in Birchler and Veitia, 2007). Again, Mendel’s careful characterization of his genetic material before making crosses likely eliminated aneuploid plants from his analyses and prevented non-Mendelian inheritance of traits resulting from extra chromosomes.

Meiotic drive

Reasons for an unequal segregation of genetic information leading to non-Mendelian inheritance are not restricted to asymmetric or irregular separation of chromosomes during meiosis. It can also occur later at the level of successive gamete formation and gamete fitness, summarized as “meiotic drive.” Meiotic drive is the overrepresentation of some gametes because of the elimination of others (Lindholm et al., 2016; Bravo Núñez et al., 2018). This may be based on positive selection of a particular genotype, for example, during egg cell specification, because only one of the four meiotic products develops into an embryo sac. In the male pathway, all four recombinant genotypes can potentially develop further, but negative selection against specific genotypes can distort the ratio of gametes represented in the mature pollen population. In angiosperms, different recombination products of the parental genome are under strong selection, as the specification of egg and sperm cells occurs during three or two post-meiotic mitotic divisions, respectively, of the gametophytes in the haploid phase of the life cycle, lacking a balancing second allele.

Cytoplasmic inheritance

Imbalance in the transfer of genetic information via the gametes can also result from differential inheritance of traits encoded in the DNA of mitochondria or chloroplasts. Although gene numbers in mitochondria and chloroplasts are small in relation to the number in the nuclear genomes, the organellar genomes contribute to important traits. With some exceptions, plastids and mitochondria are usually contributed to the embryo by the egg cell but not by the sperm (Reboud and Zeyl, 1994; Birky, 2001). Therefore, organellar genomes are inherited mainly via the maternal parent, a phenomenon that has been called cytoplasmic inheritance. The several hundred copies of organellar genomes within a cell can be genetically distinct. The complement of organelles—and their DNA—can undergo random- or selection-driven changes in relative composition. If a mutation in the chloroplast DNA renders a subset of chloroplasts defective in chlorophyll synthesis, the segregation of chloroplasts can lead to variegation, with green sectors of cells containing green chloroplasts, white sectors in which their chloroplasts cannot make chlorophyll, or intermediate sectors because they contain cells with both types (e.g. Azarin et al., 2020). Therefore, selecting “green” as a trait could have presented another potential pitfall for Mendel’s experiments of inheritance.

Agamospermy

One case of non-Mendelian inheritance indeed did irritate Mendel during his experiments with other plant species (Koltunow et al., 2011). Some seed plants produce seeds in which not only the organelles but also the nuclear genomes of the embryos are exclusively of maternal origin. This agamospermy is a version of apomixis, an asexual propagation in which segregation and recombination of the genetic material is circumvented. Among the plants that Mendel had confirmed for true breeding of convenient phenotypes like flower color were Hieracium species (hawkweed), which were only much later known to reproduce by agamospermy. Choosing Hieracium, Mendel gave up the advantage of a supportive flower morphology, as emasculation is extremely difficult in individual florets of the composite flower heads of the Asteraceae, but he was successful in cross-pollination (Berger, 2022). However, due to the different principle of seed formation, and even some co-occurrence of apomictic and sexual reproduction in these plants, the results were strongly contrasting those obtained with the pea crosses (Nogler, 2006). Even after the recognition of Mendel’s work in the early 20th century, different models of inheritance, a “Pisum type” and a “Hieracium type” were proposed, and the discrepancy was only solved after becoming aware of apomixis in seed-producing plants (cited after Nogler, 2006).

Imprinting

In his publication, Mendel emphasized that he performed all experiments in reciprocal orientation, in such a way that the maternal plant in one combination was also used as a paternal plant and pollen donor in the same combination of traits (Mendel, 1866). For the variants Mendel used and reported, it did not matter which trait was inherited from which parent. However, for different traits and other plant species, for example, the pigmentation of maize kernels, reciprocal crosses might have different results. The ability to control the dosage of the parental chromosomes to the triploid endosperm has led to the discovery of “imprinting” (Kermicle, 1970). Like paramutation, the molecular basis for imprinting lies in epigenetic control of gene activation or repression laid down in one of the parental gametes and maintained as a stable state in the resulting zygote and embryo. Later described for numerous other traits, imprinting has become a research focus in human genetics, as several genetic diseases are due to failures in correct imprinting (Sanchez-Delgado et al., 2016).

Modern models

Mendel rationally defined criteria that made P. sativum appropriate for his experiments. He was at the same time fortunate because his choice allowed him to avoid the potential pitfalls described above (except for the Hieracium experiments), without being aware of them. However, other plant species have contributed more to our concept of inheritance than pea. The role of Z. mays for the understanding of paramutation is just one example where research with this plant has allowed substantial insight into fundamental principles of plant biology, for example, development, genetic diversity, evolution, or domestication (Gaut et al., 2000; Coe, 2001; Hake and Ross-Ibarra, 2015). And it reached far beyond plants, as expressed by the Nobel Prize award for Barbara McClintock’s discovery of transposons in maize (Jones, 2005). The growing relevance of maize as a global food and feed product has of course contributed much to intensive studies how agriculturally relevant traits are inherited. Despite controversy, insect-resistant transgenic maize is one of the most widespread products of transgene technology, and maize is currently being adapted to exploit the power of gene and genome editing of its traits by the CRISPR (Clustered Regularly Interspersed Short Palindromic Repeats) principle (McCaw et al., 2020).

In the second half of the 20th century, plant geneticists turned to another genetic model plant, the thale cress A. thaliana. As a small, fast growing, commercially irrelevant dicotyledonous plant, it stands in contrast to the monocot maize in many respects, but it won over maize by the number of citations in databases when searching for connections with inheritance, genetics, or epigenetics (PubMed 12-2021). Its potential as a model plant was laid out by Friedrich Laibach (1943), in a publication reflecting on the plant traits that he considered important for planned studies on flower development. He listed similar criteria for his choice as Mendel for the peas: high fertility, culture of many plants on limited space, short generation time, available natural variation, and easy cross pollination to obtain fertile hybrids. His rationale for Arabidopsis was further strengthened by his observation of the low chromosome number (Laibach, 1907). Laibach had to leave his university position in 1945 for political reasons. It took a while till Georg Rédei (1975) recapitulated and complemented arguments that promoted Arabidopsis as a genetic tool, but his article inspired many pioneers of Arabidopsis research and resulted in a growing collection of natural variants, the first mutant collections, a recombination-based genetic map, the determination of the small genome size, and many other seminal findings (reviewed in Koornneef and Meinke, 2010; Koch, 2019). Koornneef and Meinke (2010) have pointed out that, besides of the favorable plant traits, the cooperation and community spirit of the early Arabidopsis researchers has contributed much to the unstoppable career of A. thaliana and its relatives as model organisms for genetic and molecular plant biology, a success story that had another peak in the first (nearly complete) plant genome (Initiative, 2000).

No model is perfect, and many more plant species are by now established as excellent study objects for a wide range of additional biological questions. The rapidly expanding amount of information about genes and genomes, the tools to link them with functional analyses, and the large amount of yet undiscovered diversity of plant biology guarantee that we can expect unprecedented insight into the biology of organisms that are essential for the future of the planet and our own. But we should not forget that natural evolution as well as animal and plant breeding depend on the principles of inheritance that Gregor Mendel helped us so much to understand.

Acknowledgments

The author is extremely grateful to Liam Dolan who identified lack of clarity, suggested improvements, and erased violations of the English language in the first version of the manuscript. Further thanks go to one anonymous reviewer and to Jim Birchler, who stimulated additional reflections in the final version.

Funding

Work of the author is supported by the Gregor Mendel Institute, the Austrian Academy of Sciences, and the Austrian Science Fund (FWF).

Conflict of interest statement. None declared.

 

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell) is: Ortrun Mittelsten Scheid (ortrun.mittelsten_scheid@gmi.oeaw.ac.at)

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