Abstract
Compared to controlled laboratory conditions, plant growth in the field is rarely optimal since it is frequently challenged by large fluctuations in light and temperature which lower the efficiency of photosynthesis and lead to photo‐oxidative stress. Plants grown under natural conditions therefore place an increased onus on the regulatory mechanisms that protect and repair the delicate photosynthetic machinery. Yet, the exact changes in thylakoid proteome composition which allow plants to acclimate to the natural environment remain largely unexplored. Here, we use quantitative label‐free proteomics to demonstrate that field‐grown Arabidopsis plants incorporate aspects of both the low and high light acclimation strategies previously observed in laboratory‐grown plants. Field plants showed increases in the relative abundance of ATP synthase, cytochrome b 6 f, ferredoxin‐NADP+ reductases (FNR1 and FNR2) and their membrane tethers TIC62 and TROL, thylakoid architecture proteins CURT1A, CURT1B, RIQ1, and RIQ2, the minor monomeric antenna complex CP29.3, rapidly‐relaxing non‐photochemical quenching (qE)‐related proteins PSBS and VDE, the photosystem II (PSII) repair machinery and the cyclic electron transfer complexes NDH, PGRL1B, and PGR5, in addition to decreases in the amounts of LHCII trimers composed of LHCB1.1, LHCB1.2, LHCB1.4, and LHCB2 proteins and CP29.2, all features typical of a laboratory high light acclimation response. Conversely, field plants also showed increases in the abundance of light harvesting proteins LHCB1.3 and CP29.1, zeaxanthin epoxidase (ZEP) and the slowly‐relaxing non‐photochemical quenching (qI)‐related protein LCNP, changes previously associated with a laboratory low light acclimation response. Field plants also showed distinct changes to the proteome including the appearance of stress‐related proteins ELIP1 and ELIP2 and changes to proteins that are largely invariant under laboratory conditions such as state transition related proteins STN7 and TAP38. We discuss the significance of these alterations in the thylakoid proteome considering the unique set of challenges faced by plants growing under natural conditions.
Highlights
Most of our current understanding of developmental acclimation of photosynthesis in plants is based on studies performed under controlled laboratory conditions
Low light acclimation favoring increased amounts of light harvesting antenna complex II (LHCII) and photosystem I (PSI) to maximize solar energy capture, while high light acclimation leads to increases in the abundance of ATP synthase, cytochrome b6f and ferredoxin-NADP+ reductase (FNR) complexes to maximize electron and proton transfer capacity to better utilize the available light (Bailey et al, 2001, 2004; Ballottari et al, 2007; Kouřil et al, 2013; Mikko et al, 2006; Schumann et al, 2017; Vialet-Chabrand et al, 2017; Ware et al, 2015; Wientjes et al, 2013a, 2013b)
Arabidopsis plants grown under natural field conditions show a very different phenotype to those grown under controlled laboratory conditions, differing substantially in thylakoid membrane protein composition and pigment content as well as leaf morphology (Mishra et al, 2012; Schumann et al, 2017; Wituszynska et al, 2013)
Summary
Most of our current understanding of developmental acclimation of photosynthesis in plants is based on studies performed under controlled laboratory conditions (reviewed by Schöttler & Toth, 2014; Walters, 2005). Substantial efforts have been made to better characterize the differences in thylakoid membrane protein composition and light harvesting and electron transfer function between laboratory and field grown Arabidopsis plants (Mishra et al, 2012; Schumann et al, 2017; Wituszynska et al, 2013). We address this gap in our knowledge, employing mass spectrometry to perform a label-free quantitative proteomic comparison of the thylakoid membranes of outdoor (Field)- and laboratory (Lab)-grown A. thaliana plants to further our understanding of acclimation and photoprotection in the thylakoid membrane Our study highlights those proteins and regulatory mechanisms that are instrumental in the developmental adaptation of Arabidopsis to natural conditions, providing context for our previous work on acclimation to varying growth light intensity under laboratory conditions (Flannery et al, 2021)
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