Expression of a carotenogenic gene allows faster biomass production by redesigning plant architecture and improving photosynthetic efficiency in tobacco

Abstract

SUMMARY Because carotenoids act as accessory pigments in photosynthesis, play a key photoprotective role and are of major nutritional importance, carotenogenesis has been a target for crop improvement. Although carotenoids are important precursors of phytohormones, previous genetic manipulations reported little if any effects on biomass production and plant development, but resulted in specific modifications in carotenoid content. Unexpectedly, the expression of the carrot lycopene β‐cyclase (DcLCYB1) in Nicotiana tabacum cv. Xanthi not only resulted in increased carotenoid accumulation, but also in altered plant architecture characterized by longer internodes, faster plant growth, early flowering and increased biomass. Here, we have challenged these transformants with a range of growth conditions to determine the robustness of their phenotype and analyze the underlying mechanisms. Transgenic DcLCYB1 lines showed increased transcript levels of key genes involved in carotenoid, chlorophyll, gibberellin (GA) and abscisic acid (ABA) biosynthesis, but also in photosynthesis‐related genes. Accordingly, their carotenoid, chlorophyll, ABA and GA contents were increased. Hormone application and inhibitor experiments confirmed the key role of altered GA/ABA contents in the growth phenotype. Because the longer internodes reduce shading of mature leaves, induction of leaf senescence was delayed, and mature leaves maintained a high photosynthetic capacity. This increased total plant assimilation, as reflected in higher plant yields under both fully controlled constant and fluctuating light, and in non‐controlled conditions. Furthermore, our data are a warning that engineering of isoprenoid metabolism can cause complex changes in phytohormone homeostasis and therefore plant development, which have not been sufficiently considered in previous studies.

Lycopene β-cyclase expression influences plant physiology, development, and metabolism in tobacco plants

“…Recently, a major growth advantage was reported in tobacco lines expressing the carrot DcLCYB1 (Moreno et al, 2016). This was shown under fully controlled (constant and fluctuating light regimes) and non-controlled climate conditions (Moreno et al, 2020).…”

“…Thereby, induction of leaf senescence was delayed, and mature leaves maintained a high photosynthetic capacity. This ultimately resulted in higher fitness and yield in these tobacco lines (Moreno et al, 2020).…”

“…In light of the reported growth benefit in tobacco (Moreno et al, 2020) it is of interest to understand how a single gene transformation can trigger molecular and physiological responses that are reflected in higher yield. The higher DcLCYB1 expression in the nuclear tobacco lines was reflected in 2-fold increase in β-carotene content.…”

Plant apocarotenoids: from retrograde signaling to interspecific communication

“…ABA is also necessary to generate and coordinate the plant’s response against abiotic and biotic stress factors (i.e., drought, salt and pathogens) through synergistic and antagonistic interactions with other hormones (i.e., gibberellins, ethylene and auxins) (De Vleesschauwer et al ., 2010). A recent study showed that enhanced ABA and gibberellin content accumulation through the expression of the Daucus carota (carrot) LYCOPENE β ‐CYCLASE1 ( DcLCYb1 ) leads to increased plant yield and enhanced photosynthetic efficiency in tobacco (Moreno et al ., 2020). ABA‐mediated coordination of the ripening process determines the harvest‐time and shelf‐life of horticulturally important crop plants.…”

The colour of crop improvement

“…Until now, it was unclear what caused the accelerated development and increased biomass yield in these transgenic tobacco plants. With the support of his current boss, Aleksandra Skirycz, Moreno and his colleagues report in this issue of The Plant Journal that the observed phenotype is mainly caused by altered gibberellin (GA) and abscisic acid (ABA) content (Figure; Moreno et al , 2020). They showed that the ratio of these two hormones was especially important.…”