Integrative Morphological, Physiological, Proteomics Analyses of Jujube Fruit Development Provide Insights Into Fruit Quality Domestication From Wild Jujube to Cultivated Jujube

Abstract

Jujube (Ziziphus jujuba) was domesticated from wild jujube (Z. jujuba var. spinosa). Here, integrative physiological, metabolomic, and comparative proteomic analyses were performed to investigate the fruit expansion and fruit taste components in a jujube cultivar ‘Junzao’ and a wild jujube ‘Qingjiansuanzao’ with contrasting fruit size and taste. We revealed that the duration of cell division and expansion largely determined the final fruit size, while the intercellular space in the mesocarp dictated the ratio of mesocarp volume in mature fruits. The high levels of endogenous gibbereline3 (GA) and zeatin in the growing fruit of ‘Junzao’ were associated with their increased fruit expansion. Compared with ‘Junzao,’ wild jujube accumulated lower sugars and higher organic acids. Furthermore, several protein co-expression modules and important member proteins correlated with fruit expansion, sugar synthesis, and ascorbic acid metabolism were identified. Among them, GA20OX involved in GA biosynthesis was identified as a key protein regulating fruit expansion, whereas sucrose-6-phosphate synthase (SPS) and neutral invertase (NINV) were considered as key enzymes promoting sugar accumulation and as major factors regulating the ratio of sucrose to hexose in jujube fruits, respectively. Moreover, the increase of Nicotinamide adenine dinucleotide-Malate dehydrogenase (NAD-MDH) activity and protein abundance were associated with the malic acid accumulation, and the high accumulation of ascorbic acid in wild jujube was correlated with the elevated abundance of GalDH, ZjAPXs, and MDHAR1, which are involved in the ascorbic acid biosynthesis and recycling pathways. Overall, these results deepened the understanding of mechanisms regulating fruit expansion and sugar/acids metabolisms in jujube fruit.

Shading Inhibits Sugar Accumulation in Leaf and Fruit of Jujube (Ziziphus jujuba Mill.)

“…Similar to leaf, up-regulated expression of ZjHK6 and ZjFK2 would promote hexose phosphorylation, inhibiting the accumulation of fructose and glucose in shaded fruits. Huang et al [51] believed that SPS and INV should be considered key enzymes that promote sugar accumulation in the jujube cultivar 'Junzao,' which is different from the findings in our study under low light conditions. This difference might be attributed to altered transcription levels of related genes that affect sugar accumulation, or it might be the result of cultivar differences.…”

Triterpenoids in Jujube: A Review of Composition, Content Diversity, Pharmacological Effects, Synthetic Pathway, and Variation during Domestication

“…ZJ is domesticated from wild, sour jujube. ZA has sourer, smaller, and less fleshy fruit, and it gradually evolved into ZJ with a sweet taste, large fruit, and more flesh after a long period of artificial or natural domestication [ 106 ]. Metabolomic analysis of 182 ZJ and 25 wild ZA germplasm resources identified 427 metabolites with chemical annotations, including 41 terpene metabolites, and 90 metabolites showed a decreasing pattern from wild ZA to ZJ, and the reduced metabolites were primarily rich in triterpenoids.…”

Identification of key genes controlling L-ascorbic acid during Jujube (Ziziphus jujuba Mill.) fruit development by integrating transcriptome and metabolome analysis

“…The above results suggest that these genes have an important effect on maintaining high AsA content during the early development of jujube fruit. There are two AsA synthetic pathways in jujube, and Huang’s study based on the proteomic level of jujube identified 15 proteins involved in the L-galactose pathway but no proteins related to the myo-inositol pathway ( Huang et al, 2021 ). However, notably, in our study, since the expression levels of the two isoforms of ZjMIOX genes and ZjGulLO gene in myo-inositol pathway was up-regulated from the ST3 (white-ripening stage) ( Figure 4 ), indicating that the inositol pathway may play a vital role in maintaining AsA accumulation at maturity.…”