The mechanism for brassinosteroids suppressing climacteric fruit ripening

Abstract

The plant hormone ethylene is important for the ripening of climacteric fruit, such as pear (Pyrus ussuriensis), and the brassinosteroid (BR) class of phytohormones affects ethylene biosynthesis during ripening via an unknown molecular mechanism. Here, we observed that exogenous BR treatment suppressed ethylene production and delayed fruit ripening, whereas treatment with a BR biosynthesis inhibitor promoted ethylene production and accelerated fruit ripening in pear, suggesting BR is a ripening suppressor. The expression of the transcription factor BRASSINAZOLE-RESISTANT 1PuBZR1 was enhanced by BR treatment during pear fruit ripening. PuBZR1 interacted with PuACO1, which converts 1-aminocyclopropane-1-carboxylic acid (ACC) to ethylene, and suppressed its activity. BR-activated PuBZR1 bound to the promoters of PuACO1 and of PuACS1a, which encodes ACC synthase, and directly suppressed their transcription. Moreover, PuBZR1 suppressed the expression of transcription factor PuERF2 by binding its promoter, and PuERF2 bound to the promoters of PuACO1 and PuACS1a. We concluded that PuBZR1 indirectly suppresses the transcription of PuACO1 and PuACS1a through its regulation of PuERF2. Ethylene production and expression profiles of corresponding apple (Malus domestica) homologs showed similar changes following epibrassinolide treatment. Together, these results suggest that BR-activated BZR1 suppresses ACO1 activity and the expression of ACO1 and ACS1, thereby reducing ethylene production and suppressing fruit ripening. This likely represents a conserved mechanism by which BR suppresses ethylene biosynthesis during climacteric fruit ripening.

Recent Advances in Phytohormone Regulation of Apple-Fruit Ripening

“…Brassinosteroids (BRs) are important steroid hormones that promote plant growth and development, for example, cell proliferation, pollen development, fruit ripening, and senescence [52]. The latest study showed that endogenous BRs, including typhasterol (TY), 6-deoxocastasterone (6-deoxoCS), and castasterone (CS), reduced gradually during pear (Pyrus ussuriensis) fruit development [6]. The progressive reduction of endogenous BRs during fruit development indicated that BRs might be an inhibitory factor of fruit ripening.…”

“…The application of 3 µM epibrassinolide (EBR) observably suppressed ethylene production and effectively maintained fruit firmness during the apple-fruit storage period. In contrast, a treatment of 10 µM brassinazole (Brz), an inhibitor of BR biosynthesis, evidently promoted ethylene production and decreased fruit firmness in apples [6]. In pears, exogenous EBR and Brz treatment has the same effect as in apples [6].…”

“…Knowledge on the role of phytohormones other than ethylene during apple-fruit ripening has been limited for a long time. However, an increasing number of studies point to important roles for jasmonates, auxins, brassinosteroids, and abscisic acid in apple-fruit ripening [4][5][6][7]. A better understanding of the hormone regulatory mechanisms in the ripening of apple-fruit is both biologically meaningful and economically significant for generating strategies to improve apple-fruit qualities and fruit nutrition, and reduce postharvest economic losses [8].…”

Recent Advances in the Regulation of Climacteric Fruit Ripening: Hormone, Transcription Factor and Epigenetic Modifications

“…However, treatment of tomato with the BR synthetic inhibitor brassinazole inhibited the expression of ethylene synthesis related genes and ethylene production [113] . In pear (P. ussuriensis), treatment of fruit with epibrassinolide (EBR), a brassinosteroid, significantly inhibited ethylene production and maintained fruit firmness compared with untreated control fruit during storage [114] .…”

“…Ji et al reported that endogenous BRs such as typhasterol (TY), 6-deoxocastasterone (6-deoxoCS) and castasterone (CS) gradually decreased during pear (P. ussuriensis) fruit development (Fig. 2), and treatment with 0.2, 3 or 10 µmol•L −1 EBR significantly inhibited ethylene production and well-maintained fruit firmness compared with untreated control fruit [114] . They further revealed that high concentrations of BRs activate the expression of TF PuBZR1, PuBZR1 suppresses the enzyme activity of PuACO1 by direct protein interaction in the cytoplasm, and the transcription of PuACO1 and PuACS1a in the nucleus, thereby reducing ethylene production and suppressing fruit ripening.…”