Phytohormone synthesis pathways in sweet briar rose (Rosa rubiginosa L.) seedlings with high adaptation potential to soil drought

Highlights

• Rosa rubiginosa indicates high adaptive potential to soil drought.

• 32 plant hormones were evaluated under drought stress.

• We established preferred synthesis pathways for three gibberellins, six auxins and eight cytokinins.

• Sweet briar seedlings increased gibberellin pool at the expense of reducing the pool of cytokinins and auxins.

Abstract

The study aimed to determine the phytohormone profile of sweet briar rose (Rosa rubiginosa L.) seedlings and privileged synthesis pathways of individual hormones including gibberellins, cytokinins and auxins in response to long-term soil drought. We detected eight gibberellins, nine auxins and fifteen cytokinins. Abscisic acid (ABA) was also detected as a sensitive indicator of water stress. Thirty days of soil drought induced significant increase of ABA content and species-specific quantitative changes of other phytohormones. We established preferred synthesis pathways for three gibberellins, six auxins and eight cytokinins. Both an increase and decrease in gibberellin and cytokinin levels may modulate sweet briar's response to soil water shortage. In the case of auxins, induction of effective adaptation mechanisms to extremely dry environments is mostly triggered by their rising levels. Under drought stress, sweet briar seedlings increased their gibberellin pool at the expense of reducing the pool of cytokinins and auxins. This may indicate a specific role of gibberellins in adaptation mechanisms to long-term soil water deficit developed by sweet briar.

Introduction

The global range of occurrence indicates the high adaptive potential of sweet briar rose (Rosa rubiginosa L.) to adverse environmental conditions, including soil drought. Sweet briar colonizes dry areas of South America, New Zealand, South Africa, and Australia (Hura et al., 2017; Zimmermann et al., 2010).

Plants have evolved many strategies to respond to soil drought at morphological, physiological, biochemical, and molecular level (Iqbal et al., 2019; Nxele et al., 2017; Sohag et al., 2020). At a biochemical level, plants with enhanced tolerance to long-term soil drought need particularly effective and stable adaptation mechanisms that would prevent cell desiccation and facilitate colonization of drylands (Hu and Xiong, 2014). Plant response to stress is partially regulated by genes controlling phytohormone biosynthesis (Hu and Xiong, 2014; Shinozaki and Yamaguchi-Shinozaki, 2007). Phytohormones may play both positive and negative role in plant tolerance to environmental stresses (Verma et al., 2016). An interplay between individual phytohormone groups, including a new group of plant hormones karrikins, is also of great importance and can be involved in plant drought tolerance (Antala et al., 2020; Sharma et al., 2019). In plants exposed to drought, phytohormone concentration in the cells depends on many factors such as drought duration, stress severity and ability of individual species to respond to the water stress (Hura et al., 2017; Sharma et al., 2019; Verma et al., 2016).

Abscisic acid is best recognized for its regulatory role in water stress tolerance (Hura et al., 2017; Verma et al., 2016). However, information regarding the occurrence and the role of other plant hormones (gibberellins, cytokinins, auxins) under water stress conditions is scarcely available. It has been shown that phytohormones may regulate plant response to stress factors at the last stage of cellular signal transduction by activation or deactivation of transcription factors (Kohli et al., 2018). Such an activation mechanism was confirmed for the cytokinin trans-zeatin (t-zeatin) and a transcription factor ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2) contributing specifically to Pseudomonas syringae resistance (Choi et al., 2010). Auxins also regulate plant response to soil drought by enhancing water-stress survival rates or limiting water loss (Lee et al., 2012). As far as gibberellins are concerned, their reduced concentration seems to improve plant tolerance to soil water deficit, but the mechanism of this relationship remains unclear (Nir et al., 2014). Hura et al. (2017a) demonstrated a significant increase or decrease of individual gibberellins in triticale exposed to water stress at different developmental stages.

Considering that biochemical mechanisms controlling high adaptation potential of sweet briar to drylands are still largely unknown, the study aimed to determine phytohormone profile of its seedlings and work out dominant synthesis pathways of individual gibberellins, cytokinins and auxins. We found the responses at an early growth stage of a seedling, when plants of small biomass experience long-term soil water shortage, particularly interesting. We hypothesized that the adaptation mechanism of R. rubiginosa seedlings to long-lasting soil drought involves e.g. induction of species-specific pathways of auxin, cytokinin and gibberellin synthesis.