Genetics of zonal leaf chlorosis and genetic linkage to a major gene regulating skin anthocyanin production (MdMYB1) in the apple (Malus × domestica) cultivar Honeycrisp

Abstract

‘Honeycrisp’ is a widely grown and acclaimed apple cultivar that is commonly used in breeding programs. It also has a well-documented tendency to develop the physiological disorder, zonal leaf chlorosis (ZLC). This disorder causes reduced photosynthetic capacity and is thought to be due to a problem with phloem loading, although the underlying genetics of the disorder have not previously been discerned. In order to understand the breeding implications of the disorder, six families with ‘Honeycrisp’ as a parent and one family with ‘Honeycrisp’ as both a maternal and paternal grandparent were evaluated for ZLC incidence over two years. One major quantitative trait locus (QTL) for ZLC incidence was identified on linkage group (LG) 9. A haplotype in ‘Honeycrisp’ that originated from grandparent ‘Duchess of Oldenburg’ was associated with increased ZLC incidence in offspring in both years and all families evaluated. The LG9 QTL was 5 to 10 cM from MdMYB1, which is a major gene regulating fruit skin anthocyanin production. ‘Honeycrisp’ is heterozygous for red fruit skin overcolor at MdMYB1. The ‘Honeycrisp’ haplotype at the LG9 QTL associated with increased ZLC is in linkage phase with the allele at MdMYB1 associated with red color. Selection for the red allele from ‘Honeycrisp’ at MdMYB1 will result in most offspring also inheriting the haplotype at the LG9 QTL associated with high ZLC. The occurrence of two copies of this haplotype was sub-lethal in seedlings of a family where both parents inherited both the red overcolor allele at MdMYB1 and the haplotype at the LG9 QTL associated with high ZLC. This is the first study to have identified a genetic component of ZLC with clear breeding implications.

Fire blight QTL analysis in a multi-family apple population identifies a reduced-susceptibility allele in ‘Honeycrisp’

“…Phenotypic data were only included for unselected offspring ( n = 312 in 2016 and 314 in 2017) to avoid any biases from previous breeding selection (as in van de Weg et al 20 and Verma et al 34 ). To ensure reproducibility, two replicate runs with different starting seed numbers were carried out for each year (as in van de Weg et al 20 , Verma et al 34 , and Howard et al 32 , 33 ).…”

RosBREED: bridging the chasm between discovery and application to enable DNA-informed breeding in rosaceous crops

“…comm.) Zonal leaf chlorosis Discovered, “Honeycrisp” source (LG9) 97 Peach Bacterial spot—fruit Discovered, “Clayton” source (LG1 & 6) 112 , 213 ; validated, DNA test 164 Strawberry Fruit & crown rot Validated , FaRCa1 (LB6B) 121 ; DNA test 214 Crown rot Discovered, FaRCg1 (LG6B) 122 ; DNA test 122 Root & crown rot Validated, FaRPc2 (LG7D) 123 ; DNA test 126 Red stele Validated Rpf1 215 ; DNA test 216 Angular leaf spot Validated , FaRXf1 (LG6D) 124 ; DNA tests 124 , 127 Sweet cherry Powdery mildew—fruit & foliar Discovered (fruit), validated (leaf), Pmr1 (LG5) (C. Peace, pers. comm.…”

“…Due to the importance of “Honeycrisp” as a parent in all demonstration apple breeding programs, identifying and characterizing loci for important traits heterozygous in this cultivar was a high priority. Newly identified alleles inherited from “Honeycrisp” influencing soft scald and soggy breakdown 95 , scab tolerance 96 , and zonal leaf chlorosis 97 were identified. In RosBREED 2, additional loci for resistance to two important diseases were identified.…”

Quantitative trait loci‐based genomics‐assisted prediction for the degree of apple fruit cover color

“…Minor effect QTLs are often concealed by major ones via drawing up the threshold of significance (van Ooijen et al., 2009). Therefore, when the major effect QTL for apple fruit skin coloration on chromosome 9 spanning MdMYB1 was identified in several reports, only few minor effect ones were detected (Chagné et al., 2016; Gardner et al., 2014; Howard et al., 2019; Lozano et al., 2014; Migicovsky et al., 2016). If the genotype of the major QTL is identical in a sub‐population, the genetic and environmental interactions for traits due to gene pleiotropism can be eliminated.…”

“…The red/yellow dimorphism of apple skin coloration is controlled by a single locus, Rf , and the presence of the red anthocyanin pigmentation is dominant over non‐red fruit skin (Cheng, Weeden, & Brown, 1996). The major quantitative trait loci (QTLs) linked to fruit cover color were repeatedly mapped on chromosome 09 of the apple genome via either pedigree‐based or genome wide association studies (GWAS) (Chagné et al., 2016; Gardner et al., 2014; Howard, Tillman, Vanderzande, & Luby, 2019; Kunihisa et al., 2014; Lozano et al., 2014; McClure et al., 2018; Migicovsky et al., 2016). The gene controlling apple red/yellow skin color had not been identified until the expression levels of MdMYB1/MdMYB10/MdMYBA were confirmed to be associated with anthocyanin synthesis in apple skin.…”