Abstract
Zeins are the predominant storage proteins in maize (Zea mays) seeds, while Opaque2 (O2) is a master transcription factor for zein-encoding genes. How the activity of O2 is regulated and responds to external signals is yet largely unknown. Here, we show that the E3 ubiquitin ligase ZmRFWD3 interacts with O2 and positively regulates its activity by enhancing its nuclear localization. Ubiquitination of O2 enhances its interaction with maize importin1, the α-subunit of Importin-1 in maize, thus enhancing its nuclear localization ability. We further show that ZmRFWD3 can be phosphorylated by a Suc-responsive protein kinase, ZmSnRK1, which leads to its degradation. We demonstrated that the activity of O2 responds to Suc levels through the ZmSnRK1-ZmRFWD3-O2 signaling axis. Intriguingly, we found that Suc levels, as well as ZmRFWD3 levels and the cytonuclear distribution of O2, exhibit diurnal patterns in developing endosperm, leading to the diurnal transcription of O2-regulated zein genes. Loss of function in ZmRFWD3 disrupts the diurnal patterns of O2 cytonuclear distribution and zein biosynthesis, and consequently changes the C/N ratio in mature seeds. We therefore identify a SnRK1-ZmRFWD3-O2 signaling axis that transduces source-to-sink signals and coordinates C and N assimilation in developing maize seeds.
Highlights
Seed development in crops depends on the availability of carbon (C) and nitrogen (N), supplied by the mother plant, and on the capacity of sink tissues to assimilate them
The E3 Ubiquitin Ligase ZmRFWD3 Interacts with O2 We previously screened for O2 interaction partners (Zhang et al, 2012); given the established ability of post-translational modifications to regulate the function of proteins, we were interested in O2 interaction partners known to be functionally associated with post-translational modifications (PTMs)
O2 Activity Responds to Sucrose Levels Through a SNF1-related kinase1 (SnRK1)-ZmRFWD3-O2 Signaling Axis Considering the known physiology of sucrose accumulation and the strongly sucrose-responding-based regulation of SnRK1 (Baena-Gonzalez et al, 2007; Radchuk et al, 2010; Margalha et al, 2016), we investigated whether ZmSnRK1 might regulate ZmRFWD3 and/or O2, as well as whether this regulation is dependent on sucrose signaling
Summary
Seed development in crops depends on the availability of carbon (C) and nitrogen (N), supplied by the mother plant, and on the capacity of sink tissues to assimilate them. Zein proteins comprise the largest storage reserves of N in the maize endosperm, storing 50 to 70% of total N (Mertz et al, 1964; Thompson and Larkins, 1994; Holding and Larkins, 2009; Holding and Messing, 2013). The balance of C and N in maize endosperm largely depends on the coordination of starch and zein metabolism, and C and N accumulation in developing maize endosperm is well coordinated. O2 directly regulates the transcription of both zein-coding genes and genes related to starch biosynthesis, including those encoding PPDKs and starch synthase III (SSIII) (Li et al, 2015; Zhang et al, 2016; Zhan et al, 2018)
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