Changes in biochemical properties and pectin nanostructures of juice sacs during the granulation process of pomelo fruit (Citrus grandis)
Introduction
Citrus is one of the most widely grown fruit species in the world, which gains global appreciation due to its numerous nutrients and pleasant flavor (Xia et al., 2017). However, deterioration of citrus nutrients and flavor often occurs during postharvest storage, which is largely due to the fruit senescence, especially granulation (Bartholomew, 1941, Ritenour et al., 2004). Granulation is a physiological disorder of citrus fruit species (Bartholomew, 1941, Shomer et al., 1989, Burns and Achor, 1989). When affected by granulation, disordered juice vesicles become hard, dry and exhibit rapid loss of nutrients, leading to the marketable loss of fruit value (Bartholomew, 1941, Ritenour et al., 2004). Granulation is a heavy threat to the development of citrus industry (Bartholomew, 1941, Ritenour et al., 2004, Sharma et al., 2006). We recently have reported that a total of at least 4 × 108 kg citrus fruit is affected by granulation each year in China, valued approximately 200 million US dollars (Yao, Li, Cao, Deng, & Zeng, 2020). Unfortunately, it is still lack of strategies to prevent and control citrus granulation for the industry, largely due to the fact that the driven factors for the occurrence of granulation are elusive, and also the relevant mechanism remains to be resolved.
Since the first report of citrus granulation in 1941 (Bartholomew, 1941), granulation was found to occur in various citrus species, e.g., Ponkan mandarin (Tan & Chen, 1985), grapefruit (Burns & Achor, 1989), pomelo (Shomer et al., 1989, Zhang et al., 1999). Previous researches in this field analyzed the differences between normal and granulated fruit via various aspects, such as the changes of metabolites including sugars and organic acids (Sinclair & Jolliffe, 1961), the variance of cell wall components (Burns and Achor, 1989, Shomer et al., 1989, Hwang et al., 1990), differences of gene expressions at genome-scale level, further the alteration of metabolic pathways, and the key regulators of granulation (Yao, Cao, Xie, Deng, & Zeng, 2018). These results have revealed rapid deterioration in nutrients upon granulation was, at least partially, due to the secondary cell wall synthesis. Our recent report in navel orange has suggested a regulatory network of the occurrence of citrus granulation, among which, several key transcription factors might play critical roles (Yao et al, 2020). Interestingly, a very recent report in pomelo fruit has identified an important transcription factor, CgMYB58, acting as a positive regulator of lignin synthesis during granulation (Shi, Liu, Zhang, He, & Xu, 2020).
In addition to the secondary cell wall synthesis, the metabolism of primary cell wall, especially pectin, is also related to citrus granulation (Goto, 1989, Hwang et al., 1990). Pectin is the main component in the primary cell wall and the middle lamella, which bonds adjacent cells and stabilizes the mechanical strength and physical structure of cell wall. Degradation of pectin is often associated with fruit softening during fruit ripening process, which requires a series of enzymes relating to pectin metabolism (Brummell, 2006). Pectin methylesterase (PME) removes the C-6 esterification group of polygalacturonic acid residues, yielding pectin molecules with low degree of methylation, that can be either formed so-called “egg-box” structures, or be hydrolyzed by polygalacturonase (PG) or pectin lyases (PL) (Braccini et al., 1999, Brummell and Harpster, 2001). Various enzymes related to pectin metabolism are coordinated to degrade pectin during fruit ripening and thus result in fruit softening. However, the disorder of pectin metabolism caused by physiological disorder might lead to the failure of pectin degradation, e.g., chilling may induce the flesh translucency of plum (Pan, Wang, Wang, Xie, & Cao, 2018). As a serious physiological disorder in citrus fruit, granulation results in a significant increase of hardness and an obvious juiceless taste, which is completely opposite to the mature juice sacs with soft texture and juiciness (Yao et al., 2018, Yao et al., 2020). Pectin content can be increased upon granulation in grapefruit (Hwang, Huber, & Albrigo, 1990), and Sanbokan (Goto, 1989). We recently employed the next-generation-technology-based transcriptomics and observed that the genes related to pectin metabolism were highly differentially expressed upon granulation in both Ponkan mandarin and navel orange (Yao et al., 2018, Yao et al., 2020). These data indicate that pectin metabolism is involved in citrus granulation. However, the role of pectin metabolism in granulation process and the relevant mechanism remains largely unknown.
The present study focused on the granulation of pomelo fruit, an important citrus species mainly cultivated in China with an annual output of more than 4 × 109 kg (Hung, Suh, & Wang, 2017). Granulation often occurs in pomelo fruit, causing serious deterioration of fruit quality, and further affecting marketable value. The Juice sac of pomelo fruit is relatively larger than other citrus species, which can be used as a good model system to resolve granulation at a single juice sac level. Thus, the present research was designed to employ the pomelo fruit as material to comprehensively analyze dynamic changes in fruit quality, pectin content, enzyme activities relating to pectin metabolism, calcium content, nanostructures of pectin, with the aim to elucidate the role of pectin metabolism in granulation process and the relevant mechanism.
Section snippets
Fruit materials
Red-flesh pomelo (Citrus grandis) fruit were harvested at ripening stage from an orchard in Chongqing, China. The total soluble solids (TSS) content was more than 10%, and the titratable acid (TA) content was 0.4%-0.5%. Pomelo fruit with pale-yellow color and the weight of 1.5–2 kg were selected and stored at 4–7 °C and 80–85% relative humidity (RH). After 2 months of storage, at least 300 g juice sacs of each stage were picked from more than 20 pomelo fruit with uniform size and shape, samples
Phenotypic characteristics, physiological quality, and organoleptic property of pomelo fruit during the granulation process
Our observation showed that granulated juice sacs were highly heterogenous in pomelo fruit, there were at least three types of juice sacs, which were expanded, gelated and lignified, respectively. These different types of juice sacs may represent the dynamic granulation progress of pomelo fruit, with four apparent stages, as shown in Fig. 1A and 1B. Normal juice sac could be considered to be stage I, in which the juice sac was normal and transparent, and the juice may spill out while cutting.
Heterogeneity of juice sacs during citrus granulation process
Most previous researches concerning citrus granulation mainly analyzed the differences of juice sacs between normal and granulated fruit (Sinclair and Jolliffe, 1961, Tan and Chen, 1985, Sharma et al., 2016), while did not distinguish those “granulated” juice sacs which may be at different stage of granulation. Our recent report on Ponkan and navel orange revealed that in granulated fruit, the juice vesicles may be not identical, due to considerable existence of both normal and granulated juice
Conclusion
Granulated juice sacs are highly heterogeneous, exhibiting different distinct stages including expanding, gelation and lignification. Hence, the present study was designed to employ the pomelo fruit as material to systematically analyze dynamic changes in fruit quality, pectin content, enzyme activities relating to pectin metabolism, calcium content, and pectin nanostructures. TSS, TA, AsA, and juice yield of juice sacs showed a sharp decrease since gelation stage and then through the whole
CRediT authorship contribution statement
Qiuyu Li: Conceptualization, Investigation, Writing – original draft, Methodology. Shixiang Yao: Funding acquisition, Conceptualization, Investigation, Methodology, Validation, Supervision, Writing – original draft, Writing – review & editing. Lili Deng: Methodology, Data curation, Investigation. Kaifang Zeng: Conceptualization, Investigation, Supervision.
Declaration of Competing Interest
We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with this manuscript. We have no financial and personal relationships with other people or organisations that can inappropriately influence our work.
Acknowledgements
This work was funded by the National Natural Science Foundation of China (Grant No. 32172262 and 31972131), the Fundamental Research Funds for the Central Universities (Grant No. XDJK2021F008 and XDJK2018C068).
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