Multifaceted activity of cytokinin in leaf development shapes its size and structure in Arabidopsis

Abstract

The phytohormone cytokinin has been shown to affect many aspects of plant development ranging from the regulation of the shoot apical meristem to leaf senescence. However, some studies have reported contradictory effects of cytokinin on leaf physiology. Therefore cytokinin treatments cause both chlorosis and increased greening and both lead to decrease or increase in cell size. To elucidate this multifaceted role of cytokinin in leaf development, we have employed a system of temporal controls over the cytokinin pool and investigated the consequences of modulated cytokinin levels in the third leaf of Arabidopsis. We show that, at the cell proliferation phase, cytokinin is needed to maintain cell proliferation by blocking the transition to cell expansion and the onset of photosynthesis. Transcriptome profiling revealed regulation by cytokinin of a gene suite previously shown to affect cell proliferation and expansion and thereby a molecular mechanism by which cytokinin modulates a molecular network underlying the cellular responses. During the cell expansion phase, cytokinin stimulates cell expansion and differentiation. Consequently, a cytokinin excess at the cell expansion phase results in an increased leaf and rosette size fueled by higher cell expansion rate, yielding higher shoot biomass. Proteome profiling revealed the stimulation of primary metabolism by cytokinin, in line with an increased sugar content that is expected to increase turgor pressure, representing the driving force of cell expansion. Therefore, the developmental timing of cytokinin content fluctuations, together with a tight control of primary metabolism, is a key factor mediating transitions from cell proliferation to cell expansion in leaves.

Autoregulation of RCO by Low-Affinity Binding Modulates Cytokinin Action and Shapes Leaf Diversity

“…reduced cell size and is associated with slowing down differentiation. These findings are also in line with observations that increased cytokinin levels can cause a reduction in leaf cell size [32,33]. In conclusion, RCO regulates leaf shape, at least in part, by reprogramming local CK homeostasis, thereby reducing cell growth ( Figure 6E).…”

“…These transcription factors also promote leaf complexity in a CK-related pathway that appears distinct from RCO [16,38] as it has much broader effects on leaf primordium growth [20]. CK effects on leaf cell development are multifaceted and include modulation of the rate of cell proliferation, the timing of its cessation, as well as regulation of post-mitotic growth [33,39]. Consequently, answering this question will require cell-level dissection of CK pathways at different developmental stages.…”

Steady-State Levels of Cytokinins and Their Derivatives May Serve as a Unique Classifier of Arabidopsis Ecotypes

“…ABA, total CKs, IAA 328.5% 32.1% CK non-glucosides 1038.4% 41.9% CK glucosides (12) 68.8% 66.5% All CKs (22) 72.1% 72.9% Table 3. It is well known that even minor local and transient changes in CK levels can have profound physiological effects [36][37][38][39]. Thus it is highly likely that the specificity of CK action depends to a significant extent on the determination setting of CK levels with contributions from the entire network of CK conversions.…”

Silencing ofTaCKX1mediates expression of otherTaCKXgenes to increase grain yield in wheat

“…Most of the CKs positively regulate cell division and organization of shoot stem cell centres as well as stimulating the endocycle in roots by auxin-dependent or auxin-independent mechanisms (Schaller et al, 2014). CKs are also involved in regulation of various developmental and physiological processes including size and structure during leaf development (Skalak et al, 2019), delay of senescence (Gan and Amasino, 1997; Lara et al, 2004), apical dominance (Tanaka et al, 2006), root proliferation (Werner et al, 2001; Werner et al, 2003). This regulation might occur at the posttranscriptional and/or posttranslational level (Cerny et al, 2011; Kim et al, 2012) or by modulation of context-dependent chromatin accessibility (Potter et al, 2018).…”