Apple, a member of genus Malus within the Rosaceae family, is one of the most economically important and popular temperate fruit trees worldwide. Fruit taste and their overall flavor quality is determined by the content, composition and the ratios of soluble sugars and organic acids. As an organoleptic property that determines the oral sensory perception and fruit acceptance, improving fruit taste is thus a key target in apple breeding. 

Supervised by Prof. HAN Yuepeng from Wuhan Botanical Garden, the assistant Prof. LIAO Liao, collaborated with Prof. LI Li of the Huazhong Agricultural University and Prof. HAO Yujin of the Shandong Agricultural University, identified important candidate genes controlling fruit size and taste quality and revealed a genetic roadmap for the evolution of apple domestication and improvement.   

Researchers revealed the genetic relationship between wild and cultivated apples, and identified the role of M. sieversii and M. sylvestris in the domestication of cultivated apples. They further confirmed reports by previous studies that the domesticated apple originated from M. sieversii, native to the Tian Shan Mountains of central Asia, and as it spread along the Silk Road between Asia and Europe, its genetic makeups changed due to hybridization with local crabapples such as M. sylvestris. 

The apple cultivation in China has a long history dating back over two thousand years. The dessert apple 'Nai', which originated from the M. sieversii in Xinjiang, is the oldest variety recorded in China. Interestingly, no genetic exchange between ancient European cider apples and Eastern dessert apples was observed, suggesting that these two ancient varieties might have originated from independent domestication events.   

Significant differences in fruit size and taste between wild and cultivated apples were detected. Signatures of selection for fruit acidity and size were detected during the process of both domestication and improvement, but not for fruit sugar content, which suggested that fruit size selection and acidity played greater roles in the evolution of apple fruits.    

MDSOT2 was identified to be an important transporter gene controlling apple fruit sorbitol content. Interestingly, the high accumulation of sorbitol in the apple fruits was found in 'Fuji' pedigree. Sorbitol has been shown to not only be a fresh-keeping agent for prolonging fruit shelf life, but it also has a significant positive correlation with sweetness of apples. Therefore, the high accumulation of sorbitol in fruits could be in part responsible for the long shelf life and sweet juicy taste of the 'Fuji' pedigree apple fruits. 

MDTDT is a key tonoplast transporter gene controlling citric acid content in apple, and its mutation resulted in extremely low citric acid accumulation in mature cultivated apple fruits. MA1 gene not only controls the accumulation of malic acid, but also has the pleiotropic ability to control the ratio of sugar to acid.  

In summary, selection of a single gene, MdTDT, MdSOT2, or Ma1, is sufficient to cause a dramatic decrease in the accumulation of citrate, sorbitol, or malate, respectively, whereas selection for larger fruit requires pyramiding of multiple genes with minor effects and has little hitchhiking impact on fruit taste.  

The study provides genetic basis for fruit quality improvement and unravels its evolutionary roadmap during apple domestication.  

Results were published in Molecular Plant under the title “Unraveling a genetic roadmap for improved taste in the domesticated apple”. The project was supported by the National Key R&D Program of China, the Special Fund for Strategic Pilot Technology of Chinese Academy of Sciences, the National Natural Science Foundation of China, and Overseas Construction Plan for Science and Education Base, China-Africa Center for Research and Education, Chinese Academy of Sciences.  

Proposed model for the evolution of fruit size and taste during the domestication of cultivated apples. (A) Evolutionary process of apple fruit size related to pyramiding of elite alleles of at least four genes. (B) Metabolism and accumulation of organic acid and sugar components in fruit cells of wild and cultivated apples. (Image by LIAO Liao)