Transcriptomic and hormonal dynamics in relation to adventitious rooting of two parental petunia species highlight a coordinated activation of the jasmonate and auxin pathway and important role of upper-shoot derived auxin influx

Ivona Jurenic¹Sindy Chamas¹Nicole Nagler¹Gerd Ulrich Balcke²Uwe Druege^1*

• ¹Research Centre for Horticultural Crops, University of Applied Sciences Erfurt, Erfurt, Germany
• ²Leibniz-Institut fur Pflanzenbiochemie, Halle (Saale), Germany

Introduction: Adventitious rooting of cuttings is a key developmental process for vegetative propagation of many crops that involves a phytohormone-controlled reprogramming and redifferentiation of specific cells in the stem base. The endogenous control of phytohormone action at the whole-cutting level is not completely understood. Methods: Using the genome-sequenced Petunia axillaris and P. inflata, we monitored the transcriptome of phytohormone-related genes and phytohormone levels in different cutting sections through a phytohormone-targeted microarray, RT-qPCR and LC/MS-MS and analyzed the rooting response to manipulations of auxin level and transport. Results: In the stem base of both species, genes controlling jasmonic acid (JA) biosynthesis, conjugation and signaling and encoding transcription factors of the ERF family were upregulated at 0.5 hours post excision (hpe) already and followed by increased regulation of auxin-related genes. Accordingly, JA and its physiologically active isoleucine conjugate JA-Ile accumulated transiently at 0.5 hpe, before indole-3-acetic acid (IAA) peaked at 2 hpe. Genes controlling auxin biosynthesis were mostly downregulated, whereas three IAA-LEUCINE-RESISTANT-like genes were strongly upregulated between 0.5 and 2 hpe. P. inflata's greater rooting capacity versus P. axillaris was linked to higher stem-base IAA levels (0–72 hpe), resulting in a higher IAA/cytokinin ratio and stronger upregulation of auxin-signaling genes. P. inflata showed a steeper IAA gradient between the leaves and the stem base, that was positively and negatively correlated with leaf salicylic acid and cytokinin isopentenyladenine levels, respectively and associated with exclusive upregulation of PIN-like genes in the leaves. P. axillaris showed a stronger improvement of rooting by low IAA doses than P. inflata. Blocking polar auxin transport in the upper shoot prevented rooting of both species. Discussion: The results reveal excision-triggered coordination of jasmonate and auxin pathways in the stem base, interacting with ERF transcription factors, and indicate an important role for upper shoot– derived auxin influx, potentially regulated by salicylic acid and cytokinins. Higher rooting capacity of P. inflata can be explained by the higher IAA level in the stem base. The results indicate important roles of ERF113/114, ILR-like2 and 6, PIN6, PIN-like 1/3, the PINOID gene A4A49_10797, ARF11 and several LBD genes for adventitious rooting of Petunia.