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Meiotic Mutants in Potato: Valuable Variants
Stanley J. Peloquina, Leonardo S. Boiteuxb, and Domenico Carputoca Department of Horticulture, Plant Sciences, University of Wisconsin, Madison, Wisconsin 53706-1590,
b Centro Nacional de Pesquisa de Hortaliças (CNPH)/Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), C.P. 218, 70359-970 Brasília-DF, Brazil
c Department of Agronomy and Plant Genetics, University of Naples, 80055 Portici, Italy
Corresponding author: Stanley J. Peloquin, Department of Horticulture, Plant Sciences, University of Wisconsin, 1575 Linden Dr., Madison, WI 53706-1590.
PHENOTYPIC variations in the meiotic process, under control of typical Mendelian inheritance, have been found in many plant and animal species (
 | Potato biology |
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TOP
Potato biology
Description and genetic...The cultivated potato is a tetraploid (2n = 4x = 48) with four sets of similar chromosomes (where n is the gametic chromosome number and x is the basic number). The main cultivated germplasm for long-day conditions is derived from S. tuberosum Group Tuberosum, whereas S. tuberosum Group Andigena is adapted for short-day environments. The wild tuber-bearing relatives form a polyploid series with species having 24, 36, 48, 60, and 72 chromosomes—more than 70% of them are diploids (2n = 2x = 24).
The tetrasomic inheritance of the cultivated potato is infinitely more complicated than that of 2x relatives. Fortunately, haploid plants (2n = 2x = 24) of tetraploids (2n = 4x = 48) can be obtained with ease from the cultivated tetraploids, and these haploids can be crossed to most of the diploid (2n = 2x = 24) species to capture their genetic diversity. In addition to simple disomic inheritance, the employment of haploids has the great advantage for improvement of 2x hybrid populations. These 2x hybrids obtained by this approach can be crossed to the 4x potato via functioning of 2n gametes (gametes with the sporophytic chromosome number) to obtain 4x progeny (
The occurrence of postzygotic barriers may sometimes prevent interspecific and/or interploid crosses, causing abortion of hybrid endosperm. This results in sexual isolation of a number of 2x and 4x species. The endosperm balance number (EBN) hypothesis, formulated by
| Description and genetic characteristics of meiotic mutants in potatoes |
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The mutants identified in potato affect major aspects of nuclear and cytoplasmic events during micro- and megasporogenesis. Some key characteristics of meiotic mutants should be noted: (1) Almost all of these mutant phenotypes are controlled by a single locus (2) the mutations are invariably recessive; (3) sometimes the character associated with a certain genotype fails to manifest—i.e., penetrance is not always 100%; (4) the number of meiocytes that express the parental genotype can vary from 1 to 100%—i.e., variable expressivity is the rule, not the exception, with meiotic mutants; and (5) phenotypic expression is significantly modified by genetic, environmental, and developmental factors.
| Mutants affecting microsporogenesis |
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In the normal sequence of events in microsporogenesis in Solanum species, the first meiotic division is not followed by cytokinesis, two spindles in the second division are oriented so that their poles define a tetrahedron, and cytokinesis results in a tetrad of four n microspores (Figure 1). After meiosis, the microspores separate, and each forms a male n gametophyte. In plants homozygous for the meiotic mutation parallel spindles (ps/ps), some sporocytes have parallel spindles in the second division, and after cytokinesis two 2n microspores are formed, which give rise to 2n gametophytes. A modification of this occurs when second-division spindles are tripolar, and one 2n and two n microspores are formed. Another recessive mutation, named premature cytokinesis (pc), also affects microsporogenesis. The first division in many sporocytes is followed by cytokinesis, the second division does not occur, except that chromatids fall apart, and a dyad of two 2n microspores is formed.
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The significance of the ps and pc mutations resides in their genetic consequences. The ps allele controls a process that is essentially a first-division restitution (FDR) mechanism. All loci from the centromere to the first crossover that are heterozygous in the parent remain heterozygous in the gametes. One-half of the heterozygous parental loci beyond the first crossover will be heterozygous in the gametes (in 2x Solanum species there is normally only one crossover per chromosome arm). In contrast, the mutation pc is genetically equivalent to a second-division restitution (SDR) mechanism. All the loci from the centromere to the first crossover will be homozygous in the gametes, and all loci past the first crossover that are heterozygous in the parent will remain heterozygous in the gametes. From cytological observations (e.g., chromosome structure and frequency and location of chiasmata on chromosome arms), it has been estimated that the percentage heterozygosity transmitted by the gametes is roughly 80% with FDR, in contrast to less than 40% with SDR. FDR gametes are expected to resemble each other and the parental clone from which they came. In contrast, SDR is expected to produce a heterogeneous population of highly homozygous gametes.
Another meiotic mutation, named synaptic-3 (sy-3), was found in the progeny from crosses between two diploid ps/ps clones. It is characterized by almost complete lack of chiasmata (with probably no crossing over). In some sy-3 clones, only univalents are present at metaphase I, and they are distributed randomly into telophase I nuclei. This phenomenon would ordinarily lead to almost complete male sterility. However, when the sy-3 mutation is combined with the ps mutation (i.e., double homozygous genotype sy-3/sy-3, ps/ps), a high frequency of functional 2n-pollen grains is formed. No matter how unequal the distribution of univalent chromosomes is in the first division, the parallel spindles mechanism in the second division ensures a symmetric incorporation of two sets of 12 chromosomes in each pair of 2n microspores (Figure 1). The genetic significance of this combination of meiotic mutations resides in the opportunity they provide for incorporating the almost intact genotype of the 2x parent into all the 2n gametes.
| Mutations affecting megasporogenesis |
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During normal megasporogenesis in Solanum species, the first and second meiotic divisions are each followed by cytokinesis. As a result, four n megaspores are formed (Figure 1). Three of these megaspores degenerate and one becomes the functional megaspore and, after three mitotic divisions, forms the female gametophyte. Two meiotic mutants, resulting in the formation of 2n eggs, have been identified in potato. One, named omission of the second meiotic division (os), is the predominant mechanism of 2n-egg formation in Solanum species. A second mutation was described as failure of cytokinesis (fc), which takes place after the second meiotic division and is followed by nuclear fusion. Both of these variants are genetically equivalent to SDR mechanisms. Synaptic variants such as sy-3 are also expressed in megasporogenesis, but restitution rarely results in a functional 2n megaspore. For a review of synaptic mutants in potato, see
| Use of meiotic mutants in potato breeding |
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The most significant contribution of meiotic mutants is their role as essential elements for the development of new breeding methods. The overall breeding strategy with meiotic mutants involves three main components: the wild and 2x cultivated species are the "source" of genetic diversity; haploids of Tuberosum and Andigena provide a method for "capturing" the genetic diversity; and 2n gametes are an effective and efficient way to "transmit" genetic diversity to cultivated forms. Genetic diversity includes both valuable qualitative and quantitative traits, as well as the allelic variation necessary to broaden the genetic base of the cultivated potato. The most successful new breeding scheme involves obtaining 4x progeny from 4x–2x crosses, where the 2x parent forms 2n pollen via the meiotic mutant ps. The essential ingredients of the breeding scheme, designated unilateral sexual polyploidization (USP), are illustrated in Figure 2. It is important to point out that normally, after USP, 3x plants are not recovered because the 5x endosperm associated with the 3x embryo degenerate owing to EBN unbalance. The potentially wide application of the USP scheme and the often high levels of heterosis for tuber yield are strong indicators of its effectiveness. The yield of the USP-derived progenies regularly exceeds those of their respective 4x parents (
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An alternative breeding scheme with meiotic mutants, called bilateral sexual polyploidization (BSP), involves obtaining 4x progeny from 2x–2x crosses, where one 2x parent forms 2n eggs and the other 2n pollen. The BSP strategy has great potential, providing the opportunity to incorporate (via conventional or transgenic approaches) different desirable traits in the two 2x parents and then to combine them in the 4x progeny. In addition, tuber yields of 4x progenies derived from the BSP scheme also exceed those of standard 4x cultivars (
| Germplasm transfer with meiotic mutants |
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Among economic plants, the potato is unexcelled in the abundance of related germplasm resources. Several points need particular emphasis:
- Any desirable trait for plant breeding appears to be available in related species. This includes resistance/tolerance to major biotic and abiotic stresses, important tuber quality characteristics, and all the allelic diversity needed to broaden the genetic base of the cultivated forms (
HANNEMAN 1989 ). - Potato is also the easiest organism in which to incorporate the related germplasm into cultivated forms. Cytological investigations indicated very little differentiation between the chromosomes of the cultivated potato and those of most wild relatives. For example, when haploids of the cultivated potato are crossed with 24-chromosome wild species, the F1 hybrids are vigorous and, most importantly, chromosome pairing and crossing over are essentially normal (
PELOQUIN et al. 1989A ). - The 4x–2x breeding scheme is an effective and efficient method of germplasm transfer from the cultivated and wild 2x species to 4x cultivars. The availability of so many traits in the wild germplasm, the widespread occurrence of the ps allele, the ease with which diploid 2n-gamete-producer species hybridize with 4x potato, and the ease of scaling-up interploid crosses strongly favor the 4x–2x approach as a valuable scheme for germplasm transfer. In fact, many investigators have used the USP strategy to transfer monogenic and polygenic traits from the wild germplasm to the Tuberosum gene pool (for review see
ORTIZ 1998 ).
The formation of 2n gametes also provides a useful tool for transferring genes of interest from species that have developed reproductive isolating mechanisms. Several 2x species with EBN = 1 cannot be crossed with S. tuberosum haploids or other 24-chromosome species with EBN = 2. Similarly, some 4x species with EBN = 2 (which behave as diploids) cannot be crossed with S. tuberosum (EBN = 4). Crossing schemes based upon 2n gametes, ploidy manipulations, and ploidy bridges can be successfully employed for germplasm transfer among these incongruent species. For example, transferring of genes from the frost-tolerant species S. commersonii (2n = 2x = 24, 1EBN) was performed crossing a 4x(2EBN) clone of S. commersonii with 2x(2EBN) genotypes (
| Use of meiotic mutants in genetics |
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Meiotic mutants have been used to elucidate several areas of genetic research. The first involves gene-centromere mapping by half-tetrad analysis with 4x–2x crosses, where the 2x parent forms 2n pollen by either FDR (ps/ps) or SDR (pc/pc) (
The second application involves pyramiding of distinct meiotic mutations in the same genetic background. For example, clones with the doubly homozygous genotype ps/ps, sy-3/sy-3 are able to produce 2n gametes by a mechanism equivalent to FDR without crossover (FDR-NCO). These gametes transmit the parental genotype virtually intact to their progenies. The FDR-NCO 2x clones provide a homogeneous sample of heterozygous gametes for testing the parental value of 4x clones (
Another application of meiotic mutants has been to permit genetic inference about the chromosomal (physical) location of quantitative trait loci (QTL) controlling important traits in potato. A large range of 4x cultivars was crossed with a collection of full-sib 2x clones able to transmit different fractions of their heterozygosity via 2n gametes. Tuber yield of the progenies was then determined at different environments in three continents. One group of progenies was derived from FDR with crossing-over (FDR-CO) clones, where the 2x parent transmits about 80% of the heterozygosity to the 4x progeny. The other group was derived from FDR-NCO clones in which the 2x parent transmits almost 100% of its heterozygosity and epistasis to 4x progeny. Therefore, we would expect higher yields with 100% transmission of heterozygosity vs. 80% heterozygosity. However, no significant difference in total tuber yield between the two groups has been found in any of the experiments (
Another genetic application of the meiotic mutants of the potato takes advantage of the simpler structure of 2n gametes produced by 2x genotypes, which makes quantitative genetic analyses much easier compared with the tetrasomic inheritance of the 4x potato. For example, several 4x–2x mating designs involving FDR and SDR 2n gametes have been proposed by
| Application of meiotic mutants in cytology |
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The nature of cytokinesis after the second meiotic division in microsporogenesis in dicots has been discussed for many years. The two competing hypotheses have been cell-plate formation vs. cleavage furrow formation. The meiotic mutant ps provided for an easier cytological examination of this problem compared with the normal complex tetrahedral arrangement. It was found that cytokinesis differed from both cell-plate formation and cleavage furrow (
-tubulin and F-actin in cytokinesis during microsporogenesis (
| Meiotic mutants and evolution of Solanum species |
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Polyploidy is a very important evolutionary mechanism in the Angiosperms. Likewise, polyploidization has been of considerable importance in the speciation process in potato. The ploidy level in the genus Solanum extends from 2x to 6x. Two mechanisms for the origin of polyploids have been proposed: (1) asexual by somatic doubling and (2) sexual through the functioning of 2n gametes. The genetic evidence strongly favors sexual polyploidization in Solanum species (
We hypothesized that if parallel spindles were involved in the origin of the 4x cultivated potato, then the frequency of ps allele should be higher in the 4x than in the 2x progenitors (
The high gene frequencies for meiotic mutants giving rise to 2n pollen and 2n eggs provide the opportunity for two important evolutionary events: (1) since these are inherited variations, we can have multiple origins of polyploidy and (2) they allow for continuous introgression of 2x genes into 4x and 6x gene pools. An interesting feature of the ps plants is the simultaneous production of functional n and 2n pollen. They thus have the best of all possible worlds in that n pollen allows them to hybridize with 2x and via 2n pollen with 4x and 6x plants.
The evolutionary advantage of sexual polyploidization over asexual polyploidization includes heterosis for plant vigor and yield, genetic variability, minimal inbreeding, change to establish new inter- and intralocus interactions, and high fertility. Of course, to obtain 4x offspring from a cross between two 2x individuals, both 2n pollen and 2n eggs are needed. We screened plants of 2x wild species and haploids of 4x Tuberosum for the frequency of plants producing 2n eggs by the meiotic mutant os (
During a cytogenetic investigation of intra- and interspecific F2 hybrids, abnormal meiotic behavior was found in both types of hybrids (
| Future directions |
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This Perspectives documents the value of meiotic mutants in potato research—particularly in the areas of new breeding methods, germplasm transfer from wild species to cultivated forms, and evolution of polyploid Solanum species. More important, at a recent international potato meeting held in Italy, with 570 delegates from 44 countries, it was clear that use of meiotic mutants to solve potato research problems would significantly accelerate in the future. We also believe that this broad exploitation of meiotic mutants is possible in other polysomic polyploid species such as alfalfa, clover, cassava, sweet potatoes, bananas, and sugar cane.
| ACKNOWLEDGMENTS |
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The authors are grateful to Maria Esther Fonseca and Douglas Senalik (University of Wisconsin, Madison) for their skillful help with the figures.
| LITERATURE CITED |
|---|
BUSO, J. A., L. S. BOITEUX, G. C. C. TAI, and S. J. PELOQUIN, 1999a Chromosome regions between centromeres and proximal crossovers are the physical sites of major effect loci for yield in potato: genetic analysis employing meiotic mutants. Proc. Natl. Acad. Sci. USA 96:1773-1778
BUSO, J. A., F. J. B. REIFSCHNEIDER, L. S. BOITEUX, and S. J. PELOQUIN, 1999b Effects of 2n-pollen formation by first meiotic division restitution with and without crossover on eight quantitative traits in 4x-2x potato progenies. Theor. Appl. Genet. 98:1311-1319.
BUSO, J. A., L. S. BOITEUX, and S. J. PELOQUIN, 1999c Multitrait selection system using populations with a small number of interploid (4x-2x) hybrid seedlings in potato: degree of high-parent heterosis for yield and frequency of clones combining quantitative agronomic traits. Theor. Appl. Genet. 99:81-91.
CAMADRO, E. L. and S. J. PELOQUIN, 1980 The occurrence and frequency of 2n pollen in three diploid Solanums from northwest Argentina. Theor. Appl. Genet. 56:11-17.
CARPUTO, D., A. BARONE, T. CARDI, A. SEBASTIANO, and L. FRUSCIANTE et al., 1997 Endosperm balance number manipulation for direct germplasm introgression to potato from a sexually isolated relative (Solanum commersonii Dun.). Proc. Natl. Acad. Sci. USA 94:12013-12017
DAWE, R. K., 1998 Meiotic chromosome organization and segregation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:371-395.
DEN NIJS, T. P. M. and S. J. PELOQUIN, 1977 2n gametes in potato species and their function in sexual polyploidization. Euphytica 26:585-600.
GENUALDO, G., A. ERRICO, A. TIEZZI, and C. CONICELLA, 1998 -Tubulin and F-actin distribution during microsporogenesis in a 2n pollen producer of Solanum.. Genome 41:636-641.
GOLUBOVSKAYA, I. N., and A. S. MASHNENKOV, 1985 The cytogenetic evidence of the gene control of meiosis, pp. 723–738 in Pollen: Biology and Implications for Plant Breeding, edited by D. L. MULCAHY and E. OTTAVIANO. Elsevier, New York.
HANNEMAN, R. E., JR., 1989 Potato germplasm resources. Am. Potato J. 66:655-668.
HAWLEY, R. S., 1993 Meiosis is an "M" thing: twenty years of meiotic mutants in Drosophila. Genetics 135:613-618[Medline].
IWANAGA, M. and S. J. PELOQUIN, 1982 Origin and evolution of cultivated tetraploid potatoes via 2n gametes. Theor. Appl. Genet. 61:161-169.
JOHNSTON, S. A., T. M. DEN NIJS, S. J. PELOQUIN, and R. E. HANNEMAN, JR., 1980 The significance of genic balance to endosperm development in interspecific crosses. Theor. Appl. Genet. 57:5-9.
JONGEDIJK, E. and M. S. RAMANNA, 1988 Synaptic mutants in potato, Solanum tuberosum L. I. Expression and identity of genes for desynapsis. Genome 30:664-670.
KAUL, M. L. K. and T. G. K. MURTHY, 1985 Meiotic mutants in higher plants. Theor. Appl. Genet. 70:449-466.
LINDSEY, D., 1999 Larry Sandler: personal recollections. Genetics 151:1233-1237
MENDIBURU, A. O. and S. J. PELOQUIN, 1979 Gene-centromere mapping by 4x-2x matings in potato. Theor. Appl. Genet. 54:177-180.
MOK, D. W. S. and S. J. PELOQUIN, 1975 Breeding value of 2n pollen (diplandroids) in tetraploid x diploid crosses in potatoes. Theor. Appl. Genet. 46:307-314.
ORTIZ, R., 1998 Potato breeding via ploidy manipulation. Plant Breed. Rev. 16:15-86.
PELOQUIN, S. J., 1983 Genetic engineering with meiotic mutants, pp. 311–316 in Pollen: Biology and Implications for Plant Breeding, edited by D. L. MULCAHY and E. OTTAVIANO. Elsevier Science, Amsterdam.
PELOQUIN, S. J., S. H. JANSKY, and G. L. YERK, 1989a Potato cytogenetics and germplasm utilization. Am. Potato J. 66:629-638.
PELOQUIN, S. J., G. L. YERK, J. E. WERNER, and E. DARMO, 1989b Potato breeding with haploids and 2n gametes. Genome 31:1000-1004.
STELLY, D. M., 1983 (I) 2n female gametophytes in potato; and (II) Microsporocyte cytokinesis in potato. Ph.D. Thesis, University of Wisconsin-Madison.
TAI, G. C. C., 1994 Use of 2n gametes, pp. 109–132, in Potato Genetics, edited by J. E. BRADSHAW and G. R. MACKAY. CAB International, Wallingford, UK.
TAI, G. C. C. and H. DE JONG, 1997 A comparison of performance of tetraploid progenies produced by diploid and their vegetatively doubled (tetraploid) counterpart parents. Theor. Appl. Genet. 94:303-308.
WANG, H., and S. J. PELOQUIN, 1999 Phenotypic and cytogenetic analyses of F2 progenies among four Argentine 2x species. Proceedings of the 14th Trien. Conf. Euro. Assoc. for Potato Res., Sorrento, Italy, May 2–7, 1999, pp. 572–573.
WERNER, J. E. and S. J. PELOQUIN, 1991 Occurrence and mechanisms of 2n egg formation in 2x potato. Genome 34:975-982.
ZIMNOCH-GUZOWSKA, E., M. SIECZKA, H. JAKUCZUN and L. DOMANSKY, 1999 Diploid and tetraploid parental line breeding focused on resistance to pathogens and quality traits. Proceedings of the 14th Trien. Conf. Euro. Assoc. for Potato Res., Sorrento, Italy, May 2–7, 1999, pp. 329–330.
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