PbGA2ox8 induces vascular-related anthocyanin accumulation and contributes to red stripe formation on pear fruit

Rui Zhai,Richard Espley,Zhongying Wu,Chengquan Yang,Xieyu Li,Qingmei Guan,Kui Lin-Wang,Zhigang Wang,Lingfei Xu,Fengwang Ma,Jianlong Liu,Pengmin Li

doi:10.1038/s41438-019-0220-9

Rui Zhai, Richard Espley + Show 10 more

Open Access

https://doi.org/10.1038/s41438-019-0220-9

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Abstract

Fruit with stripes, which are generally longitudinal, can occur naturally, but the bioprocesses underlying this phenomenon are unclear. Previously, we observed an atypical anthocyanin distribution that caused red-striped fruit on the spontaneous pear bud sport “Red Zaosu” (Pyrus bretschneideri Rehd.). In this study, comparative transcriptome analysis of the sport and wild-type “Zaosu” revealed that this atypical anthocyanin accumulation was tightly correlated with abnormal overexpression of the gene-encoding gibberellin (GA) 2-beta-dioxygenase 8, PbGA2ox8. Consistently, decreased methylation was also observed in the promoter region of PbGA2ox8 from “Red Zaosu” compared with “Zaosu”. Moreover, the GA levels in “Red Zaosu” seedlings were lower than those in “Zaosu” seedlings, and the application of exogenous GA4 reduced abnormal anthocyanin accumulation in “Red Zaosu”. Transient overexpression of PbGA2ox8 reduced the GA4 level and caused anthocyanin accumulation in pear fruit skin. Moreover, the presence of red stripes indicated anthocyanin accumulation in the hypanthial epidermal layer near vascular branches (VBs) in “Red Zaosu”. Transient overexpression of PbGA2ox8 resulting from vacuum infiltration induced anthocyanin accumulation preferentially in calcium-enriched areas near the vascular bundles in pear leaves. We propose a fruit-striping mechanism, in which the abnormal overexpression of PbGA2ox8 in “Red Zaosu” induces the formation of a longitudinal array of anthocyanin stripes near vascular bundles in fruit.

Highlights

Fruit with stripes, which generally run longitudinally, can occur naturally
We propose a fruit-striping mechanism, in which the abnormal overexpression of PbGA2ox[8] in “Red Zaosu” induces the formation of a longitudinal array of anthocyanin stripes near vascular bundles in fruit
26 overlapping differentially expressed genes (DEGs) were screened from the anthocyanin-enriched tissues between “Red Zaosu” and “Zaosu” (Fig. 2a; Supplementary Datasets S1, S2)

Summary

Introduction

Fruit with stripes, which generally run longitudinally, can occur naturally. Alternating dark and light-green stripes are common in watermelon, pumpkin, and squash. Such stripes form along the main carpellary vascular bundles[1,2], the molecular mechanism of stripe formation has not been investigated. Unlike the common green stripes in watermelon, red stripes sometimes occur in apple, pear, and peach. Anthocyanins accumulate in flowers to attract insects for pollen dispersal or in fruit to attract animals for seed dispersal and are produced in plants as radical scavengers in response to various biotic and abiotic stresses[6,7]. The signaling networks behind the developmental and environmental regulation of anthocyanin biosynthesis are complex. The ubiquitin E3 ligase CONSTITUTIVE PHOTOMORPHOGENIC1, ELONGATED HYPOCOTYL5, and PHYTOCHROME-INTERACTING FACTOR 3 are key components involved in the regulation of light-dependent

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