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Article|01 Jun 2022|OPEN
Coordinated transcriptional regulation of the carotenoid biosynthesis contributes to fruit lycopene content in high-lycopene tomato genotypes
James R. Duduit1 ,† , Pawel Z. Kosentka1 ,† , Morgan A. Miller1 , Barbara Blanco-Ulate2 , Marcello S. Lenucci3 , Dilip R. Panthee4 , Penelope Perkins-Veazie5 and Wusheng Liu,1 ,
1Department of Horticultural Science, North Carolina State University, Raleigh, NC, 27607, USA
2Department of Plant Sciences, University of California, Davis, CA, 95616, USA
3Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento (DiSTeBA), Via Prov.le Lecce-Monteroni, Lecce, 73100 Italy
4Department of Horticultural Science, North Carolina State University, Mountain Horticultural Crops Research and Extension Center, Mills River, NC 28759, USA
5Department of Horticultural Science, Plants for Human Health Institute, North Carolina State University, North Carolina Research Campus, Kannapolis, NC 28081, USA
*Corresponding author. E-mail: wliu25@ncsu.edu
Both authors contributed equally to the study.

Horticulture Research 9,
Article number: uhac084 (2022)
doi: https://doi.org/10.1093/hr/uhac084
Views: 149

Received: 01 Nov 2021
Accepted: 25 Mar 2022
Published online: 01 Jun 2022

Abstract

Lycopene content in tomato fruit is largely under genetic control and varies greatly among genotypes. Continued improvement of lycopene content in elite varieties with conventional breeding has become challenging, in part because little is known about the underlying molecular mechanisms in high-lycopene tomatoes (HLYs). We collected 42 HLYs with different genetic backgrounds worldwide. High-performance liquid chromatography (HPLC) analysis revealed lycopene contents differed among the positive control wild tomato Solanum pimpinellifolium, HLYs, the normal lycopene cultivar “Moneymaker”, and the non-lycopene cultivar NC 1Y at the pink and red ripe stages. Real-time RT-PCR analysis of expression of the 25 carotenoid biosynthesis pathway genes of each genotype showed a significantly higher expression in nine upstream genes (GGPPS1GGPPS2GGPPS3TPT1SSU IIPSY2ZDSCrtISO and CrtISO-L1 but not the well-studied PSY1PDS and Z-ISO) at the breaker and/or red ripe stages in HLYs compared to Moneymaker, indicating a higher metabolic flux flow into carotenoid biosynthesis pathway in HLYs. Further conversion of lycopene to carotenes may be prevented via the two downstream genes (β-LCY2 and ε-LCY), which had low-abundance transcripts at either or both stages. Additionally, the significantly higher expression of four downstream genes (BCH1ZEPVDE, and CYP97C11) at either or both ripeness stages leads to significantly lower fruit lycopene content in HLYs than in the wild tomato. This is the first systematic investigation of the role of the complete pathway genes in regulating fruit lycopene biosynthesis across many HLYs, and enables tomato breeding and gene editing for increased fruit lycopene content.