Abstract
Due to their sessile nature, plants rely on root systems to mediate many biotic and abiotic cues. To overcome these challenges, the root proteome is shaped to specific responses. Proteome-wide reprogramming events are magnified in meristems due to their active protein production. Using meristems as a test system, here, we study the major rewiring that plants undergo during cold acclimation. We performed tandem mass tag-based bottom-up quantitative proteomics of two consecutive segments of barley seminal root apexes subjected to suboptimal temperatures. After comparing changes in total and ribosomal protein (RP) fraction-enriched contents with shifts in individual protein abundances, we report ribosome accumulation accompanied by an intricate translational reprogramming in the distal apex zone. Reprogramming ranges from increases in ribosome biogenesis to protein folding factors and suggests roles for cold-specific RP paralogs. Ribosome biogenesis is the largest cellular investment; thus, the vast accumulation of ribosomes and specific translation-related proteins during cold acclimation could imply a divergent ribosomal population that would lead to a proteome shift across the root. Consequently, beyond the translational reprogramming, we report a proteome rewiring. First, triggered protein accumulation includes spliceosome activity in the root tip and a ubiquitous upregulation of glutathione production and S-glutathionylation (S-GSH) assemblage machineries in both root zones. Second, triggered protein depletion includes intrinsically enriched proteins in the tip-adjacent zone, which comprise the plant immune system. In summary, ribosome and translation-related protein accumulation happens concomitantly to a proteome reprogramming in barley root meristems during cold acclimation. The cold-accumulated proteome is functionally implicated in feedbacking transcript to protein translation at both ends and could guide cold acclimation.
Highlights
Cereals face two kinds of low-temperature challenges
Our results indicate that cold acclimation triggers a drop in protein content in barley root tips, while specific proteins are accumulated
We found specific accumulation of cold markers such as COR/LEA proteins that also accumulate in mature tissues such as cereal crowns during cold
Summary
Cereals face two kinds of low-temperature challenges. The first is vernalization (Chouard, 1960; Von Zitzewitz et al, 2005; Deng et al, 2015), which is bound to seasonal climate and acts as a cue to induce the transition from vegetative to reproductive development. Plants acclimate to low temperatures using a systemic response (Hincha and Zuther, 2020) that ranges from hormonal, auxin-dependent signaling (Shibasaki et al, 2009; Rahman, 2013), through primary metabolism (Kaplan et al, 2004; Zuther et al, 2019; Erban et al, 2020), and to membrane-lipidome compositional changes (Uemura et al, 1995; Cheong et al, 2019, 2020). Long-term responses are less well understood and could partially rely on more permanent changes, for instance, by including altered protein translation or ribosomes as a main hub of the cold response or memory (Beine Golovchuk et al, 2018; GarciaMolina et al, 2020; Cheong et al, 2021)
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