Abstract
Dormancy and reducing sugar content in tubers are important traits of potato and are typical quantitative traits. Deciphering the genetic basis of potato tuber dormancy and reducing sugar content is a prerequisite for improving the two traits. DorB5.3, a stable major dormancy QTL (quantitative trait locus) previously mapped across seven environments, has been found to co-localize with REC_B_05-1, a QTL controlling reducing sugar content in potato tubers. In order to determine whether DorB5.3 was a pleiotropic QTL or not, a conditional QTL mapping was carried out, and the results suggested that DorB5.3 and REC_B_05-1 were the same QTL, controlling the dormancy and reducing sugar content in potato tubers simultaneously. Conditional QTL mapping also uncovered three pairs of epistatic QTLs which were independent of the reducing sugar content and were significant for deciphering the genetic basis of dormancy. Five genes were picked out as putative causal genes controlling DorB5.3, according to the genome annotation and transcriptomic data. The pleiotropic DorB5.3 along with the negative correlation between the causal and resultant traits provided a possibility that potato breeders could prolong the dormancy period and scale back the reducing sugar content of potato tubers in one breeding program. The results of this study could pave a way for understanding the genetic basis of both dormancy and reducing sugar content in potato breeding programs.
Similar content being viewed by others
Data Availability
The data supporting the findings of this study are available within its supplementary TableS1-2 or available from the corresponding author, BN, upon reasonable request.
References
Abbasi K, Masud T, Ali S, Khan SU, Mahmood T, Qayyum A (2015) Sugar-starch metabolism and antioxidant potential in potato tubers in response to different antisprouting agents during storage. Potato Res 58:361–375. https://doi.org/10.1007/s11540-015-9306-4
Baldermann S, Homann T, Neugart S, Chmielewski F, Götz K, Gödeke K, Huschek G, Morlock G, Rawel H (2018) Selected plant metabolites involved in oxidation-reduction processes during bud dormancy and ontogenetic development in sweet cherry buds (Prunus avium L.). Molecules 23:1197. https://doi.org/10.3390/molecules23051197
Bisognin D, Manrique-Carpintero N, Douches D (2018) QTL analysis of tuber dormancy and sprouting in potato. Am J Potato Res 95:374–382. https://doi.org/10.1007/s12230-018-9638-0
Campbell M, Suttle J, Douches D, Buell C (2014) Treatment of potato tubers with the synthetic cytokinin 1-(α-ethylbenzyl)-3-nitroguanidine results in rapid termination of endodormancy and induction of transcripts associated with cell proliferation and growth. Funct Integr Genomics 14:789–799. https://doi.org/10.1007/s10142-014-0404-1
Chmielewski F, Götz K, Homann T, Huschek G, Rawel H (2017) Identification of Endodormancy Release for Cherries (Prunus avium L.) by Abscisic Acid and Sugars. J Hortic 4:210. https://www.longdom.org/open-access/identification-of-endodormancy-release-for-cherries-prunus-avium-l-by-abscisic-acid-and-sugars-16547.html (Accessed March 23, 2022)
Cui F, Li J, Ding A, Zhao C, Wang L, Wang X, Li S, Bao Y, Li X, Feng D, Kong L, Wang H (2011) Conditional QTL mapping for plant height with respect to the length of the spike and internode in two mapping populations of wheat. Theor Appl Genet 122:1517–1536. https://doi.org/10.1007/s00122-011-1551-6
Daniels-Lake B, Pruski K, Prange R (2011) Using ethylene gas and chlorpropham potato sprout inhibitors together. Potato Res 54:223–236. https://doi.org/10.1007/s11540-011-9188-z
Fan X, Cui F, Ji J, Zhang W, Zhao X, Liu J, Meng D, Tong Y, Wang T, Li J (2019) Dissection of pleiotropic QTL regions controlling wheat spike characteristics under different nitrogen treatments using traditional and conditional QTL mapping. Front Plant Sci 10:187. https://doi.org/10.3389/fpls.2019.00187
Freyre R, Warnke S, Sosinski B, Douches DS (1994) Quantitative trait locus analysis of tuber dormancy in diploid potato (Solanum spp.). Theor Appl Genet 89:474–480. https://doi.org/10.1007/BF00225383
Garg V, Hackel A, Kühn C (2021) Expression level of mature miR172 in wild type and StSUT4 -silenced plants of Solanum tuberosum is sucrose-dependent. Int J Mol Sci 22:1455. https://doi.org/10.3390/ijms22031455
Hara-Skrzypiec A, Śliwka J, Jakuczun H, Zimnoch-Guzowska E (2018) QTL for tuber morphology traits in diploid potato. J Appl Genet 59:123-132. https://doi.org/10.1007/s13353-018-0433-x
Hou J, Zhang H, Liu J, Reid S, Liu T, Xu S, Sonnewald TZ, U, Song B, Xie C, (2017) Amylases StAmy23, StBAM1 and StBAM9 regulate cold-induced sweetening of potato tubers in distinct ways. J Exp Bot 68:2317–2331. https://doi.org/10.1093/jxb/erx076
Hou J, Liu T, Reid S, Zhang H, Peng X, Sun K, Du J, Sonnewald U, Song B (2019) Silencing of α-amylase StAmy23 in potato tuber leads to delayed sprouting. Plant Physiol Biochem 139:411–418. https://doi.org/10.1016/j.plaphy.2019.03.044
Kleinkopf G, Oberg N, Olsen N (2003) Sprout inhibition in storage: current status, new chemistries and natural compounds. Am J Pot Res 80:317. https://doi.org/10.1007/BF02854316
Li J, Lindqvist-Kreuze H, Tian Z, Liu J, Song B, Landeo J, Portal L, Gastelo M, Frisancho J, Sanchez L, Meijer D, Xie C, Bonierbale M (2012) Conditional QTL underlying resistance to late blight in a diploid potato population. Theor Appl Genet 124:1339–1350. https://doi.org/10.1007/s00122-012-1791-0
Li J, Xie C, Tian Z, Lindqvist-Kreuze H, Bonierbale M, Liu J (2015) SSR and e-PCR provide a bridge between genetic map and genome sequence of potato for marker development in target QTL region. Am J Potato Res 92:312–317. https://doi.org/10.1007/s12230-015-9432-1
Li J, Huang W, Cao H, Xiao G, Zhou J, Xie C, Xia J, Song B (2018) Additive and epistatic QTLs underlying the dormancy in a diploid potato population across seven environments. Sci Hortic 240:578–584. https://doi.org/10.1016/j.scienta.2018.06.071
Li N, Shi J, Wang X, Liu G, Wang H (2014) A combined linkage and regional association mapping validation and fine mapping of two major pleiotropic QTLs for seed weight and silique length in rapeseed (Brassica napus L.). BMC Plant Biol 14:114. https://doi.org/10.1186/1471-2229-14-114
Liu G, Yang J, Xu H, Hayat Y, Zhu J (2008) Genetic analysis of grain yield conditioned on its component traits in rice (Oryza sativa L.). Aust J Agr Res 59:189–195. https://doi.org/10.1071/AR07163
Liu X, Chen L, Shi W, Xu X, Li Z, Liu T, He Q, Xie C, Nie B, Song B (2021) Comparative transcriptome reveals distinct starch-sugar interconversion patterns in potato genotypes contrasting for cold-induced sweetening capacity. Food Chem 334:127550. https://doi.org/10.1016/j.foodchem.2020.127550
Naz R, Li M, Ramzan S, Li G, Liu J, Cai X, Xie C (2018) QTL mapping for microtuber dormancy and GA3 content in a diploid potato population. Biol Open 7:bio027375. https://doi.org/10.1242/bio.027375
Ramaraj R, Bhuyar P, Intarod K, Sameechaem N, Unpaprom Y (2021) Stimulation of natural enzymes for germination of mimosa weed seeds to enhanced bioethanol production. 3 Biotech 11:307. https://doi.org/10.1007/s13205-021-02859-9
Schuler G (1997) Sequence mapping by electronic PCR. Genome Res 7:541–550. https://doi.org/10.1101/gr.7.5.541
Scott A, Knott M (1974) A cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507–512. https://doi.org/10.2307/2529204
Simko I, McMurry S, Yang H, Manschot A, Davies P, Ewing EE (1997) Evidence from polygene mapping for a causal relationship between potato tuber dormancy and abscisic acid content. Plant Physiol 115:1453–1459. https://doi.org/10.1104/pp.115.4.1453
Sliwka J, Wasilewicz-Flis I, Jakuczun H, Gebhardt C (2008) Tagging quantitative trait loci for dormancy, tuber shape, regularity of tuber shape, eye depth and flesh colour in diploid potato originated from six Solanum species. Plant Breed 127:49–55. https://doi.org/10.1111/j.1439-0523.2008.01420.x
Suffle J, Campbell M, Olsen N (2016) Potato tuber dormancy and postharvest sprout control. In: Postharvest Ripening Physiology of Crops. CRC Press, pp 449–476. https://pennstate.pure.elsevier.com/en/publications/potato-tuber-dormancy-and-postharvest-sprout-control (Accessed March 23, 2022)
Suttle J (2004) Physiological regulation of potato tuber dormancy. Am J Potato Res 81:253–262. https://doi.org/10.1007/BF02871767
Tosetti R, Waters A, Chope G, Cools K, Alamar M, McWilliam S, Thompson A, Terry L (2021) New insights into the effects of ethylene on ABA catabolism, sweetening and dormancy in stored potato tubers. Postharvest Biol Technol 173:111420. https://doi.org/10.1016/j.postharvbio.2020.111420
Van den Berg J, Ewing E, Plaisted R, McMurry S, Bonierbale M (1996) QTL analysis of potato tuber dormancy. Theor Appl Genet 93:317–324. https://doi.org/10.1007/BF00223171
Van Ooijen J (2009) MapQTL®6, Software for the mapping of quantitative trait in experiment populations of diploid species. Kyazma B. V., Wageningen. https://www.kyazma.nl/index.php/MapQTL/Manual/ (Accessed March 23, 2022)
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Wang L, Cui F, Wang J, Jun L, Ding A, Zhao C, Li X, Feng D, Gao J, Wang H (2012) Conditional QTL mapping of protein content in wheat with respect to grain yield and its components. J Genet 91:303–312. https://doi.org/10.1007/s12041-012-0190-2
Warnes G, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B, Galili T (2020) Various R Programming Tools for Plotting Data, Version 311. https://github.com/talgalili/gplots (Accessed March 23, 2022)
Xiao G, Huang W, Cao H, Tu W, Wang H, Zheng X, Liu J, Xie C, Song B (2018) Genetic loci conferring reducing sugar accumulation and conversion of cold-stored potato tubers revealed by QTL analysis in a diploid population. Front Plant Sci 9:315. https://doi.org/10.3389/fpls.2018.00315
Yan J, Zhu J, He C, Benmoussa M, Wu P (1998) Molecular dissection of developmental behavior of plant height in rice (Oryza sativa L.). Genetics 150:1257–1265. https://doi.org/10.1093/genetics/150.3.1257
Yang J, Zhu J, Williams R (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536. https://doi.org/10.1093/bioinformatics/btm143
Zhao J, Becker H, Zhang D, Zhang Y, Ecke W (2006) Conditional QTL mapping of oil content in rapeseed with respect to protein content and traits related to plant development and grain yield. Theor Appl Genet 113:33–38. https://doi.org/10.1007/s00122-006-0267-5
Zhu J (1995) Analysis of conditional genetic effects and variance components in developmental genetics. Genetics 141:1633–1639. https://doi.org/10.1093/genetics/141.4.1633
Zhu Z, Hayart Y, Yang J, Cao L, Lou X, Xu H (2012) Statistical method for mapping QTLs for complex traits based on two backcross populations. Chin Sci Bull 57:2645–2654. https://doi.org/10.1007/s11434-012-5279-8
Funding
This work was supported by Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization (No. 201931603), the National Natural Science Foundation of China (No. 32060504), the High-level Nurturing Project of Huanggang Normal University (No. 04201711403), the Innovative Training Program for College Students of Hubei Province (202110514024), and the China Agriculture Research System of MOF and MARA (CARS-09-P07).
Author information
Authors and Affiliations
Contributions
All the authors contributed to the study conception and design. The conditional QTL mapping was conducted by Jingcai Li. The reducing sugar contents were measured by Guilin Xiao and Wei Tu. The cluster heatmap analysis was conducted by Tengfei Liu. Identification of the putative causal genes and reverse e-PCR analysis were conducted by Huoyun Chen and Wentao Tao. Bihua Nie and Botao Song conceived and planned the study. Jingcai Li and Botao Song edited and finalized the manuscript. The first draft of the manuscript was written by Jingcai Li and Wei Tu, and all the authors commented on previous versions of the manuscript. All the authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, J., Tu, W., Xiao, G. et al. Pleiotropic QTL Underlying the Dormancy and Reducing Sugar Content in Potato Tubers Uncovered by Conditional QTL Analysis. Potato Res. 66, 965–979 (2023). https://doi.org/10.1007/s11540-022-09606-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11540-022-09606-4