Disruption of the Auxin Gradient in the Abscission Zone Area Evokes Asymmetrical Changes Leading to Flower Separation in Yellow Lupine

Abstract

How auxin transport regulates organ abscission is a long-standing and intriguing question. Polar auxin transport across the abscission zone (AZ) plays a more important role in the regulation of abscission than a local concentration of this hormone. We recently reported the existence of a spatiotemporal sequential pattern of the indole-3-acetic acid (IAA) localization in the area of the yellow lupine AZ, which is a place of flower detachment. In this study, we performed analyses of AZ following treatment with an inhibitor of polar auxin transport (2,3,5-triiodobenzoic acid (TIBA)). Once we applied TIBA directly onto the AZ, we observed a strong response as demonstrated by enhanced flower abscission. To elucidate the molecular events caused by the inhibition of auxin movement, we divided the AZ into the distal and proximal part. TIBA triggered the formation of the IAA gradient between these two parts. The AZ-marker genes, which encode the downstream molecular components of the inflorescence deficient in abscission (IDA)-signaling system executing the abscission, were expressed in the distal part. The accumulation of IAA in the proximal area accelerated the biosynthesis of abscisic acid and ethylene (stimulators of flower separation), which was also reflected at the transcriptional level. Accumulated IAA up-regulated reactive oxygen species (ROS) detoxification mechanisms. Collectively, we provide new information regarding auxin-regulated processes operating in specific areas of the AZ.

Drought Disrupts Auxin Localization in Abscission Zone and Modifies Cell Wall Structure Leading to Flower Separation in Yellow Lupine

“…One of the most important phytohormones involved in abscission-related processes in yellow lupine flowers is auxin [ 6 , 7 ]. At the same time, auxins are crucial players in cell wall remodeling events as they promote divisions, growth, and differentiation [ 25 ].…”

“…In our recent report, we determined the precise localization of IAA in the floral AZ of yellow lupine [ 6 ]. Further investigation revealed the presence of asymmetrical changes in both parts of the AZ structure in response to the disruption of polar auxin transport across the AZ, which is a factor evoking flower separation [ 7 ]. It is generally accepted that the higher level of IAA above the AZ (in the pedicel) than below (in the stem fragment) prevents organs abscission [ 38 ].…”

“…It is generally accepted that the higher level of IAA above the AZ (in the pedicel) than below (in the stem fragment) prevents organs abscission [ 38 ]. All factors perturbing the natural balance of this hormone, e.g., artificial AZ activation by organ removal, direct IAA application, or treatment with TIBA (2,3,5-triiodobenzoic acid, polar auxin transport inhibitor), activate the AZ [ 6 , 7 , 39 , 40 ]. A similar effect is observed here, in our presented investigation, in which we provide novel facts about auxin involvement in stress-induced abscission processes.…”

“…Therefore, it cannot be excluded that the IAA accumulation, presented here, during the drought in the AZ ( Figure 2 B) is evoked by formed ET [ 3 ]. On the other hand, there are some reports suggesting the enhanced sensitivity of AZ cells in response to the disruption of natural IAA balance in different plant species [ 38 , 48 ], including lupine [ 6 , 7 ]. It is even more complicated given the case of Populus , in which IAA acts independently of ET in organ abscission [ 49 ].…”

“…At the same time, biosynthesis of the main hormonal stimulators of flower abscission, abscisic acid (ABA), and ethylene (ET) is stimulated [ 3 , 5 ]. As we have already proven, the functioning of the lupine AZ and, as a consequence, flower separation is also determined by a spatial and temporal distribution of indole-3-acetic acid (IAA) in different regions of the AZ, which is maintained by the interactions with ET [ 6 , 7 ]. In turn, the ET role, as the main effector of abscission, is to activate hydrolytic enzymes, responsible for cell wall remodeling that causes middle lamella hydrolysis and, finally, organ separation [ 8 , 9 , 10 ].…”