Coordinating the morphogenesis-differentiation balance by tweaking the cytokinin-gibberellin equilibrium

Abstract

Morphogenesis and differentiation are important stages in organ development and shape determination. However, how they are balanced and tuned during development is not fully understood. In the compound leaved tomato, an extended morphogenesis phase allows for the initiation of leaflets, resulting in the compound form. Maintaining a prolonged morphogenetic phase in early stages of compound-leaf development is dependent on delayed activity of several factors that promote differentiation, including CIN-TCP transcription factor (TF) LA, the MYB TF CLAU and the plant hormone Gibberellin (GA). Here, we investigated the genetic regulation of the morphogenesis-differentiation balance by studying the relationship between LA, CLAU and GA. Our genetic and molecular examination suggest that LA is expressed more broadly than CLAU and determines the spatio-temporal context of CLAU activity. We demonstrate that both LA and CLAU affect the Cytokinin/Gibberellin (CK/GA) balance. LA reduces the sensitivity of the leaf margin to CK, shown before to be also affected by CLAU. CLAU affects leaf active GA content and sensitivity, shown previously to be also influenced by LA. Therefore, LA and CLAU likely function in parallel pathways to promote leaf differentiation by converging on common downstream processes, including the CK/GA balance.

Cytokinin- microbiome interactions regulate developmental functions

“…Treatment with bacterial isolates increased the number of leaves produced ( Figure 3C ). We therefore chose to examine leaf development, which follows a predictable and well characterized program in S. lycopersicum M82 (Shani et al, 2010; Israeli et al, 2021), in depth. For this, we selected the B. megaterium isolate 4C, which consistently performed best in growth promotion assays we conducted ( Figure 3 ).…”

“…To further characterize the effect of bacterial isolates on development, we next examined the expression of a variety of developmental genes. We chose genes related to boundary definition, which is important for organ initiation (Steiner et al, 2020; Bar et al, 2016), meristem maintenance, which is important for increased morphogenesis (Israeli et al, 2021), and, given the TCSv2 activation results, genes of the CK pathway. We found that the bacilli isolates exclusively activated CK pathway genes ( Figure 5A-E ), with B. megaterium 4C not surprisingly activating more CK pathway genes than B. pumilus R2E.…”

“…The KNOXI gene Tkn2 , plays important role in promoting leaf morphogenesis by delaying differentiation, preserving the meristematic identity of the leaf margin. The NAM-CUC transcription factor GOBLET determines boundaries within meristematic regions, that are necessary for organ initiation (Berger et al, 2009; Bar et al, 2016) While the MYB transcription factor CLAU regulates the exit from the morphogenetic phase of tomato leaf development by affecting the CK/ GA balance (Israeli et al, 2021). The changes in the expression levels of these genes upon treatment with bacilli isolated from high-CK genotypes ( Figure 5 ) further supports the notion that these particular bacilli isolates boost the leaf morphogenetic potential, in part through the promotion of CK signaling.…”

“…Thus, it is not surprising that changing endogenous CK content or signaling would cause alterations to plant development, resulting in changes to organ structure and patterning. CK has been demonstrated to promote morphogenesis and delay differentiation during plant development in many different plant species and developmental contexts (DeMason, 2005; Nikolić et al, 2006; Marsch-Martínez et al, 2012; Li et al, 2013; Israeli et al, 2021), likely by delaying the differentiation of meristematic cells (Bartrina et al, 2011). Tomato plants with altered CK content have altered developmental programs, and modified organ structures.…”

A cell wall-associated gene network shapes leaf boundary domains

“…Yet, it was shown that CK promotes cell proliferation and that reduced CK levels lead to a decrease in cell divisions and consequently to smaller organs (Holst et al, 2011). Moreover, a recent study revealed that a CK/GA balance is responsible for leaf complexity in tomato as it controls morphogenesis/differentiation switch (Israeli et al, 2021). Hence, it is also possible that CK signaling is partially impaired in the spy-3 mutant and as a consequence modifies the serration growth dynamics.…”