Correspondence between maturity date and molecular variations in a NAC transcription factor of diploid and polyploid <i>Prunus</i> species
The maturity date (MD) of Prunus stone fruit has been long known to be a quantitatively inherited trait. A NAC-type gene
indicated as PpNAC1 (ppa008301m) has been found recently to be a strong candidate of a major gene influencing MD in peach. A
9-bp insertion in this gene resulted in earlier MD in two segregating peach populations. This study was carried out to test whether this
mutation in the PpNAC1 gene can be used as a reliable functional marker for MD in a wide range of peach cultivars of various origins
and phenotypic characters. A total of 125 peach cultivars were examined using a 3 × 3 custom chi-square contingency table according
to their NAC genotype and MD (early, midseason, and late). Cramér's V equaled 0.478 and the Goodman-Kruskal index (l) was 0.37,
indicating an extremely strong correlation between MD and NAC genotype. In addition, we determined 15 sequences from 10 cultivars
of five Prunus species including peach, almond, apricot, sour cherry, and European plum with E-values ranging from 9e-88 to 2e-74,
supporting their homology to PpNAC1. A total of 69 single nucleotide polymorphisms and two insertion/deletions were detected in the
coding region of the partial NAC domain sequences with three mutations putatively inducing nonconservative amino acid replacements
and a nonsense mutation in specific alleles of early ripening apricot and sour cherry cultivars. The results are discussed with focus on
the putative molecular mechanisms of mutations in the NAC genes, crop evolutionary perspectives, and the opportunities for designing
cost-efficient markers to predict MD in Prunus breeding programs.
___
- Aida M, Ishida T, Tasaka M (1999). Shoot apical meristem and
cotyledon formation during
Arabidopsis
embryogenesis:
interaction among the
CUP-SHAPED COTYLEDON
and
SHOOT MERISTEMLESS
genes. Development 126: 1563-1570.
- Akagi T, Hanad, T, Yaegaki H, Gradzie, TM, Tao R (2016). Genome-
wide view of genetic diversity reveals paths of selection and
cultivar differentiation in peach domestication. DNA Res 23:
271-282.
- Baker VS, Imade GE, Molta NB, Tawde P, Pam SD, Obadofin MO,
Sagay SA, Egah DZ, Iya D, Afolabi BB et al. (2008). Cytokine-
associated neutrophil extracellular traps and antinuclear
antibodies in
Plasmodium falciparum
infected children under
six years of age. Malaria J 7: 1.
- Bianchi VJ, Rubio M, Trainotti L, Verde I, Bonghi C, Martínez-Gómez
P (2015).
Prunus
transcription factors: breeding perspectives.
Front Plant Sci 6: 443.
- Cramér H (1946). Mathematical Methods of Statistics. Princeton, NJ,
USA: Princeton University Press.
Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A,
Plomion C, Monet R (1999). Mapping QTLs controlling fruit
quality in peach (
Prunus persica
(L.) Batsch). Theor Appl Genet
98: 18-31.
- Dirlewanger E, Quero-García J, Le Dantec L, Lambert P, Ruiz D,
Dondini L, Illa E, Quilot-Turion B, Audergon JM, Tartarini S
et al. (2012). Comparison of the genetic determinism of two
key phenological traits, flowering and maturity dates, in three
Prunus
species: peach, apricot and sweet cherry. Heredity 109:
280-292.
- Dondini L, Lain O, Geuna F, Banfi R, Gaiotti F, Tartarini S, Bassi D,
Testolin R (2007). Development of a new SSR-based linkage
map in apricot and analysis of synteny with existing
Prunus
map. Tree Genet Genomes 3: 239-249.
- Eduardo I, Pacheco I, Chietera G, Bassi D, Pozzi C, Vecchietti A,
Rossini L (2011). QTL analysis of fruit quality traits in two
peach intraspecific populations and importance of maturity
date pleiotropic effect. Tree Genet Genomes 7: 323-335.
- Eduardo I, Picañol R, Rojas E, Batlle I, Howad W, Aranzana MJ,
Arús P (2015). Mapping of a major gene for the slow ripening
character in peach: co-location with the maturity date gene and
development of a candidate gene-based diagnostic marker for
its selection. Euphytica 205: 627-636.
- Giovannoni JJ (2004). Genetic regulation of fruit development and
ripening. Plant Cell 16: S170-S180.
- Halász J, Hegedűs A, Hermán R, Stefanovits-Bányai É, Pedryc A
(2005). New self-incompatibility alleles in apricot (
Prunus
armeniaca
L.) revealed by stylar ribonuclease assay and
S
-PCR
analysis. Euphytica 14: 57-66.
- Halász J, Kodad O, Hegedűs A (2014). Identification of a recently
active
Prunus
‐specific non‐autonomous
Mutator
element with
considerable genome shaping force. Plant J 79: 220-231.
- Hall TA (1999). BioEdit: a user-friendly biological sequence
alignment editor and analysis program for Windows 95/98/
NT. Nucl Acids Symp Ser 41: 95-98.
- Mohácsy M (1954). Őszibaracktermesztés. Budapest, Hungary:
Mezőgazdasági Kiadó (in Hungarian).
Montgomery SB, Goode DL, Kvikstad E, Albers CA, Zhang ZD,
Mu XJ, Ananda G, Howie B, Karczewski KJ, Smith KS et al.
(2013). The origin, evolution, and functional impact of short
insertion–deletion variants identified in 179 human genomes.
Genome Res 23: 749-761.
- Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala
R, Schäffer AA (2008). Database indexing for production
MegaBLAST searches. Bioinformatics 15: 1757-1764.
- Nuñez-Lillo G, Cifuentes-Esquivel A, Troggio M, Micheletti D,
Infante R, Campos-Vargas R, Orellana A, Blanco-Herrera F,
Meneses C (2015). Identification of candidate genes associated
with mealiness and maturity date in peach [
Prunus persica
(L)
Batsch] using QTL analysis and deep sequencing. Tree Genet
Genomes 11: 1-13.
- Olmstead JW, Sebolt AM, Cabrera A, Sooriyapathirana SS, Hammar
S, Iriarte G, Wang D, Chen CY, Van der Knaap E, Iezzoni AF
(2008). Construction of an intra-specific sweet cherry (
Prunus
avium
L) genetic linkage map and synteny analysis with the
Prunus
reference map. Tree Genet Genomes 4: 897-910.
- Olsen AN, Ernst HA, Leggio LL, Skriver K (2005). NAC transcription
factors: structurally distinct, functionally diverse. Trends Plant
Sci 10: 79-87.
- Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara
K, Osato N, Kawai J, Carninci P et al. (2003). Comprehensive
analysis of
NAC
family genes in
Oryza sativa
and
Arabidopsis
thaliana
. DNA Res 10: 239-247.
- Patthy L (2008). Protein Evolution. 2nd ed. Oxford, UK: Blackwell.
Pirona R, Eduardo I, Pacheco I, Linge CDS, Miculan M, Verde
I, Tartarini S, Dondini L, Pea G, Bassi D et al. (2013). Fine
mapping and identification of a candidate gene for a major
locus controlling maturity date in peach. BMC Plant Biol 13:
166.
- Quilot B, Wu BH, Kervella J, Genard M, Foulongne M, Moreau K
(2004). QTL analysis of quality traits in an advanced backcross
between
Prunus persica
cultivars and the wild relative species
P
davidiana
. Theor Appl Genet 109: 884-897.
- Ramming DW (1991). Genetic control of a slow-ripening fruit trait
in nectarine. Can J Plant Sci 71: 601-603.
- Rapaics R (1940). A magyar gyümölcs. Budapest, Hungary: Királyi
Magyar Természettudományi Társulat (in Hungarian).
- Romeu JF, Monforte AJ, Sánchez G, Granell A, García-Brunton J,
Badenes ML, Ríos G (2014). Quantitative trait loci affecting
reproductive phenology in peach. BMC Plant Biol 14: 52.
- Sablowski RW, Meyerowitz EM (1998). A homolog of
NO APICAL
MERISTEM
is an immediate target of the floral homeotic genes
APETALA3/PISTILLATA
. Cell 92: 93-103.
- Salazar JA, Ruiz D, Campoy JA, Tartarini S, Dondini L, Martínez-
Gómez P (2016). Inheritance of reproductive phenology traits
and related QTL identification in apricot. Tree Genet Genomes
12: 1-14.
- Shan W, Kuang JF, Chen L, Xie H, Peng HH, Xiao YY, Li XP, Chen
WX, He QG, Chen JY et al. (2012). Molecular characterization
of banana NAC transcription factors and their interactions
with ethylene signalling component EIL during fruit ripening.
J Exp Bot 63: 5171–5187.
- Shen ZJ, Confolent C, Lambert P, Poëssel JL, Quilot-Turion B, Yu ML,
Ma RJ, Pascal T (2013). Characterization and genetic mapping
of a new blood-flesh trait controlled by the single dominant
locus
DBF
in peach. Tree Genet Genomes 9: 1435-1446.
- Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996). The
no apical meristem gene of
Petunia
is required for pattern
formation in embryos and flowers and is expressed at meristem
and primordia boundaries. Cell 85: 159-170.
- Sun L, Huang L, Hong Y, Zhang H, Song F, Li D (2015).
Comprehensive analysis suggests overlapping expression of
rice ONAC transcription factors in abiotic and biotic stress
responses. Int J Mol Sci 16: 4306-4326.
- Takada S, Hibara KI, Ishida T, Tasaka M (2001). The
CUP-SHAPED
COTYLEDON1
gene of
Arabidopsis
regulates shoot apical
meristem formation. Development 128: 1127-1135.
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S
(2011). MEGA5: molecular evolutionary genetics analysis
using maximum likelihood, evolutionary distance, and
maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
- Thompson JD, Higgins DG, Gibson TJ (1994). CLUSTAL W:
improving the sensitivity of progressive multiple sequence
alignment through sequence weighting, position-specific gap
penalties and weight matrix choice. Nucleic Acids Res 22:
4673-4680.
- Tóth MG (1997). Meggy. In: Tóth MG, editor. Gyümölcsészet.
Budapest, Hungary: Primon Kiadó, Nyíregyháza, pp. 257-271
(in Hungarian).
- Tsukamoto T, Hauck NR, Tao R, Jiang N, Iezzoni AF (2006). Molecular
characterization of three non-functional
S
-haplotypes in sour
cherry (
Prunus cerasus
). Plant Mol Biol 62: 371-383.
- Wang N, Zheng Y, Xin H, Fang L, Li S (2013). Comprehensive
analysis of NAC domain transcription factor gene family in
Vitis vinifera
. Plant Cell Rep 32: 61-75.
- Zhou H, Lin‐Wang K, Wang H, Gu C, Dare AP, Espley RV, He H,
Allan AC, Han Y (2015). Molecular genetics of blood‐fleshed
peach reveals activation of anthocyanin biosynthesis by NAC
transcription factors. Plant J 82: 105-121.