Guanosine tetraphosphate (ppGpp) accumulation inhibits chloroplast gene expression and promotes super grana formation in the moss Physcomitrium (Physcomitrella) patens

Abstract

The nucleotides guanosine tetraphosphate and pentaphosphate (or ppGpp) are implicated in the regulation of chloroplast function in plants. ppGpp signalling is best understood in the model vascular plant Arabidopsis thaliana where it acts to regulate plastid gene expression to influence photosynthesis, plant development and immunity. However, little is known about the conservation or diversity of ppGpp signaling in other land plants.• We studied the function of ppGpp in the moss Physcomitrium (previously Physcomitrella) patens using an inducible system for triggering ppGpp accumulation. We used this approach to investigate the effects of ppGpp on chloroplast function, photosynthesis and growth.• We demonstrate that ppGpp accumulation causes a dramatic drop in photosynthetic capacity by inhibiting chloroplast gene expression. This was accompanied by the unexpected reorganisation of the thylakoid system into super grana. Surprisingly, these changes did not affect gametophore growth, suggesting that bryophytes and vascular plants may have different tolerances to defects in photosynthesis.• Our findings point to the existence of both highly conserved and more specific targets of ppGpp signalling in the land plants that may reflect different growth strategies.

New perspectives on the molecular mechanisms of stress signalling by the nucleotide guanosine tetraphosphate (ppGpp), an emerging regulator of photosynthesis in plants and algae

“…Although the (p)ppGpp pathway was discovered some time ago in plants and algae, it is only recently that significant progress has been made in understanding its physiological roles. Progress has come principally from manipulating ppGpp levels in vivo (pppGpp is not usually detected in plants) via the use of different RSH mutants or the expression of ppGpp synthetases and hydrolases initially in Arabidopsis (Maekawa et al ., 2015 ; Yamburenko et al ., 2015 ; Sugliani et al ., 2016 ; Abdelkefi et al ., 2018 ; Honoki et al ., 2018 ; Ono et al ., 2020 ; Goto et al ., 2022 ; Romand et al ., 2022 ), and more recently using similar approaches in rice, moss and algae (Imamura et al ., 2018 ; Avilan et al ., 2021 ; Harchouni et al ., 2022 ; Ito et al ., 2022 ; Li et al ., 2022 ). These studies have highlighted the role of (p)ppGpp signalling in regulating chloroplast function (and in particular photosynthesis) during growth and development, acclimation to nitrogen starvation, and the onset of night and immune responses (Fig.…”

“…A common theme emerging from multiple studies on plants and algae is that manipulation of ppGpp levels alters photosynthetic activity. Specifically, ppGpp accumulation causes a decrease in photosynthesis – reducing maximal quantum efficiency ( F v / F m ) and operating efficiency (or quantum yield) and electron transport rate (Sugliani et al ., 2016 ; Honoki et al ., 2018 ; Avilan et al ., 2021 ; Harchouni et al ., 2022 ; Ito et al ., 2022 ; Li et al ., 2022 ; Romand et al ., 2022 ). In Arabidopsis, moss and diatoms, these changes are associated with modifications in the architecture of the photosynthetic electron transport chain.…”

“…In Arabidopsis, moss and diatoms, these changes are associated with modifications in the architecture of the photosynthetic electron transport chain. Notably at photosystem II (PSII), there is a decrease in the quantity of PSII reaction centres compared with the peripheral light‐harvesting antenna (Maekawa et al ., 2015 ; Sugliani et al ., 2016 ; Avilan et al ., 2021 ; Harchouni et al ., 2022 ). Photosystem I (PSI) would appear to be less affected, although more work is required to determine the relative impact of ppGpp on PSI and PSII.…”

“…Photosystem I (PSI) would appear to be less affected, although more work is required to determine the relative impact of ppGpp on PSI and PSII. Rubisco levels also drop markedly in response to ppGpp accumulation, and RSH mutants deficient in (p)ppGpp metabolism show defects in nitrogen remobilisation from Rubisco during stress‐induced senescence (Maekawa et al ., 2015 ; Sugliani et al ., 2016 ; Honoki et al ., 2018 ; Harchouni et al ., 2022 ; Li et al ., 2022 ; Romand et al ., 2022 ). Interestingly, while the decrease in photosynthetic activity in response to ppGpp accumulation is conserved, certain features vary.…”

“…Such effects might be expected given the role of (p)ppGpp in the regulation of photosynthetic activity as discussed earlier. However, the situation is complex because (p)ppGpp overaccumulation in plants including Arabidopsis, rice and moss has variously been reported to increase (Maekawa et al ., 2015 ), decrease (Sugliani et al ., 2016 ; Li et al ., 2022 ) or have no detectable effect on plant size (Harchouni et al ., 2022 ; Ito et al ., 2022 ). These conflicting results may be related to differing levels of (p)ppGpp, species‐specific effects, differences in light intensity/quality and nutrient levels.…”