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Molecular Markers Improve Breeding Efficiency in Apomictic Poa Pratensis L

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Molecular Markers Improve Breeding Efficiency in Apomictic Poa Pratensis L agronomy Review Molecular Markers Improve Breeding Efficiency in Apomictic Poa Pratensis L. B. Shaun Bushman 1,*, Alpana Joshi 1 and Paul G. Johnson 2 1 Forage and Range Research Laboratory, USDA-ARS, Logan, UT 84322-6300, USA; [email protected] 2 Department of Plants, Soils, and Climate, Utah State University, Logan, UT 84322-4820, USA; [email protected] * Correspondence: [email protected]; Tel.: +1-435-797-2901 Received: 6 December 2017; Accepted: 5 February 2018; Published: 10 February 2018 Abstract: Kentucky bluegrass (Poa pratensis L.) is a highly adapted and important turfgrass species in cool-season climates. It has high and variable polyploidy, small and metacentric chromosomes, and a facultative apomictic breeding system. As a result of the polyploidy and apomixis, identifying hybrids for Mendelian selection, identifying fixed apomictic progeny of desirable hybridizations for cultivar development, or differentiating among cultivars with subtle phenotypic differences is challenging without the assistance of molecular markers. Herein, we show data and review previous research showing the uses and limitations of using molecular markers for hybrid detection, apomixis assessment, and cultivar discrimination. In order to differentiate among different apomictic offtypes, both molecular markers and flow cytometry are necessary. For assessing similarity among progeny of hybridizations, as well as discriminating among cultivars, sets of markers are necessary and cryptic molecular variation must be considered. High throughput genotyping platforms are critical for increased genotyping efficiency. Keywords: Kentucky bluegrass; Poa pratensis; molecular marker; turfgrass; apomixis 1. Introduction The Poa genus comprises approximately 500 species, depending on taxonomic sources [1]. It is a highly adaptable genus, spanning all continents and diverse habitats. There are caespitose species used for rangeland restoration, such as P. secunda [2] and P. densa [3]. There are weedy species like P. annua, whose presence is so pervasive that it is begrudgingly used in lawns and golf courses [4]. Other species have limited or strategic value as turfgrasses, such as P. trivialis [5] and P. arachnifera [6]. The most important agronomic species in the genus is P. pratensis, commonly called Kentucky bluegrass in the USA and smooth-stalked meadowgrass in Europe. Kentucky bluegrass is an interesting organism from a genetic perspective. It has high and variable polyploidy, ranging generally from 8× to 14× with a base number of seven. Although abundant, the Kentucky bluegrass chromosomes are mostly metacentric and relatively small, obfuscating attempts to karyotype or count the exact chromosome numbers under a microscope (Figure1) and leading to high frequencies of aneuploids during meiosis or mitosis [7,8]. Thus, based on results from both chromosome counts and flow cytometry, Kentucky bluegrass progenies and cultivars have been presented as mean or approximate chromosome numbers rather than exact numbers [7–11]. The epigenetic consequences of high and variable ploidy crosses and progeny are unknown, as are the identity and putative activity of transposable elements. Agronomy 2018, 8, 17; doi:10.3390/agronomy8020017 www.mdpi.com/journal/agronomy Agronomy 2018, 8, 17 2 of 8 Agronomy 2018, 8, x FOR PEER REVIEW 2 of 8 Figure 1. Example of two Simple Sequence Repeat (SSR) markers amplified on two Kentucky Figure 1. Example of two Simple Sequence Repeat (SSR) markers amplified on two Kentucky bluegrass bluegrass parents and 12 of their progeny: (a) maternal parent, (b) paternal parent, (c–g) putative parents and 12 of their progeny: (a) maternal parent, (b) paternal parent, (c–g) putative apomictic apomictic progeny showing maternal genotypes for both SSR markers, (h–j) hybrid progeny carrying progeny showing maternal genotypes for both SSR markers, (h–j) hybrid progeny carrying at least one at least one paternal allele for at least one of the SSR markers, (k) polyhaploid progeny validated paternal allele for at least one of the SSR markers, (k) polyhaploid progeny validated through flow through flow cytometry that may show band loss, and (l–n) progeny with non-maternal genotypes cytometry that may show band loss, and (l–n) progeny with non-maternal genotypes but maternal but maternal cytotypes (small-scale aneuploid or self-pollination progeny). cytotypes (small-scale aneuploid or self-pollination progeny). Additionally, Kentucky bluegrass is a facultative apomict, exhibiting sporophytic gametogenesisAdditionally, to produce Kentucky unreduced bluegrass isgametes, a facultative pseudogam apomict,ous exhibiting use of pollen sporophytic for viable gametogenesis endosperm todevelopment produce unreduced, and parthenogenesis gametes, pseudogamous to skip fertilization use of [12] pollen. Apomixis for viable can endosperm come through development, the female andand/or parthenogenesis male lines, is almost to skip never fertilization 100% efficient, [12]. Apomixis and results can in come highly through-polyploid, the femalefixed heterozygotes. and/or male lines,Although is almost apomixi nevers is 100% predominant efficient, andin most results crosses in highly-polyploid,, five types of apomicitic fixed heterozygotes. offtypes have Although been apomixispostulated is and predominant reported [9] in: mostpolyhaploids, crosses, five BII hybrids types of (‘B’ apomicitic standing offtypes for ‘bastard’) have, been BIII hybrids postulated through and reportedthe male [or9]: female polyhaploids, line, and BII BhybridsIV hybrids (‘B’ ( standingTable 1). forCombined ‘bastard’), with BIII aneuploidy,hybrids through these the apomictic male or femaleofftypes line, result and in BseveralIV hybrids sources (Table of 1genetic). Combined and genomic with aneuploidy, variation, only these one apomictic of which offtypescorresponds result to ina ‘normal’ several sourceshybrid ofin geneticthe classical and genomic sense of variation, reduction, only segregation one of which, and correspondsindependent to assortment a ‘normal’. hybridDifferent in thegenetic classical backgrounds sense of reduction, show respective segregation, predominance and independents for certain assortment. offtypes, Different and in genetic each backgroundsgeneration or showunder respectiveenvironmental predominances stresses thefor frequency certain offtypes,of those offtypes and in each can change generation (Table or 2 under). For environmentalKentucky bluegrass stresses breeders, the frequency an understanding of those offtypes of the cannature change and (Tablefrequency2). For of Kentuckyapomixis offtypes bluegrass is breeders,critical to anunderstand understanding the uniformity of the nature and andstability frequency of nascent of apomixis breeding offtypes lines. is critical to understand the uniformity and stability of nascent breeding lines. Table 1. Apomict and ‘offtype’ progeny possibilities from Kentucky bluegrass hybridization events. Table 1. Apomict and ‘offtype’ progeny possibilities from Kentucky bluegrass hybridization events. Progeny Type Maternal Gamete 1 Paternal Gamete Fusion Method Embryo Ploidy 2 Endosperm Ploidy 3 Apomict unreduced -- Parthenogenesis 2C 5C (6C) Progeny Type Maternal Gamete 1 Paternal Gamete Fusion Method Embryo Ploidy 2 Endosperm Ploidy 3 Polyhaploid reduced -- Parthenogenesis C 3C (4C) Apomict unreduced – Parthenogenesis 2C 5C (6C) BII hybrid reduced reduced Fertilization 2C 3C Polyhaploid reduced – Parthenogenesis C 3C (4C) BIII hybrid (M) 4 unreduced reduced Fertilization 3C 5C BII hybrid reduced reduced Fertilization 2C 3C 4 BBIIIIII hybridhybrid (P) (M) reducedunreduced unreduced reduced Fertilization Fertilization 3C 3C 4C 5C BBIVIII hybridhybrid (P)unreduced reduced unreduced unreduced Fertilization Fertilization 4C 3C 6C 4C BIV hybrid unreduced unreduced Fertilization 4C 6C 1 reduced gametes occur through meiosis while unreduced occur through apospory; 2 embryo C-value 1 reduced gametes occur through meiosis while unreduced occur through apospory; 2 embryo C-value is based on parentalis based ploidyon parental numbers ploidy of 2n numbers (not 2× in of polyploids). 2n (not 2× Additionally,in polyploids) in. Kentucky Additionally, bluegrass, in Kentucky the numbers bluegrass, will not bethe exact numbers due to will aneuploidy; not be exact3 endosperm due to aneuploidy can develop; through 3 endosperm pseudogamy can develop or double through fertilization, pseudogamy resulting or in 4 endospermdouble fertilization, C-values from resulting reduced in or endosperm (unreduced) C paternal-values gametes; from reduced(M) corresponds or (unreduced) to maternal paternal source gametes while (P); corresponds to paternal. 4 (M) corresponds to maternal source while (P) corresponds to paternal. Agronomy 2018, 8, 17 3 of 8 Table 2. Apomict and offtype frequencies from three reciprocal Kentucky bluegrass crosses determined through SSR marker genotyping and flow cytometry. Ninety-six seeds were germinated from each cross, and numbers tested that are less than 96 represent seedling mortality. Progeny NorthStar PI371768 × Washington PI440603 × PI499557 × PI440603 × Type × PI371768 NorthStar × PI440603 Washington PI440603 PI499557 Apomict 78 91 67 88 83 86 Polyhaploid 3 0 10 3 1 2 BII Hybrid 1 0 0 1 0 0 BIII Hybrid 1 0 0 3 3 0 Total Tested 83 91 77 95 87 88 Because of the low frequency of hybrids and otherwise unpredictable nature of offtypes, breeding of Kentucky bluegrass has mainly relied on ecotype selection rather than Mendelian selection [13]. In
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