Cytokinin and CLE signaling are highly intertwined developmental regulators across tissues and species

Cammarata, Joseph; Roeder, Adrienne; Scanlon, Michael J.

doi:10.1016/j.pbi.2019.05.006

Cited by 18 publications

(12 citation statements)

References 82 publications

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“…In addition, more complex signaling cascades combining both signals acting immediately at fertilization and signals whose range increases with cell size would be described by this model 3, again because valve epidermal cells do not divide. For many critical plant and animal developmental programs, the correct final morphogenetic output results from the combinatorial effect of a number of signaling pathways and growth (97,(103)(104)(105)(106)(107)(108)(109)(110)(111)(112)(113). Indeed, based on our modeling and experimental data, the growth dynamics of the postfertilized fruit seems to be no exception.…”

Section: Computational Modeling Predicts Mobility Properties Of the Smentioning

confidence: 85%

Growth dynamics of the Arabidopsis fruit is mediated by cell expansion

Ripoll

Zhu

Brocke

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Fruit have evolved a sophisticated tissue and cellular architecture to secure plant reproductive success. Postfertilization growth is perhaps the most dramatic event during fruit morphogenesis. Several studies have proposed that fertilized ovules and developing seeds initiate signaling cascades to coordinate and promote the growth of the accompanying fruit tissues. This dynamic process allows the fruit to conspicuously increase its size and acquire its final shape and means for seed dispersal. All these features are key for plant survival and crop yield. Despite its importance, we lack a high-resolution spatiotemporal map of how postfertilization fruit growth proceeds at the cellular level. In this study, we have combined live imaging, mutant backgrounds in which fertilization can be controlled, and computational modeling to monitor and predict postfertilization fruit growth in Arabidopsis. We have uncovered that, unlike leaves, sepals, or roots, fruit do not exhibit a spatial separation of cell division and expansion domains; instead, there is a separation into temporal stages with fertilization as the trigger for transitioning to cell expansion, which drives postfertilization fruit growth. We quantified the coordination between fertilization and fruit growth by imaging no transmitting tract (ntt) mutants, in which fertilization fails in the bottom half of the fruit. By combining our experimental data with computational modeling, we delineated the mobility properties of the seed-derived signaling cascades promoting growth in the fruit. Our study provides the basis for generating a comprehensive understanding of the molecular and cellular mechanisms governing fruit growth and shape.

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Section: Computational Modeling Predicts Mobility Properties Of the Smentioning

confidence: 85%

Growth dynamics of the Arabidopsis fruit is mediated by cell expansion

Ripoll

Zhu

Brocke

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…The hormone cytokinin promotes SAM formation in both Arabidopsis and Physcomitrium 30 . Several lines of evidence suggest an antagonistic relationship between CLV1 and RPK2, and cytokinin 16,22 . In moss shoots, cytokinin promotes the formation of new SAMs 23 , while loss of CLV1 or RPK2 signaling causes ectopic stem cell formation 16 .…”

Section: Introductionmentioning

confidence: 99%

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

Cammarata

Farfan

Scanlon

et al. 2021

Preprint

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Plant shoots grow from stem cells within Shoot Apical Meristems (SAMs), which produce lateral organs while maintaining the stem cell pool. In the model flowering plant Arabidopsis, the CLAVATA (CLV) pathway functions antagonistically with cytokinin signaling to control the size of the multicellular SAM via negative regulation of the stem cell organizer WUSCHEL (WUS). Although comprising just a single cell, the SAM of the model moss Physcomitrium patens (formerly Physcomitrella) performs equivalent functions during stem cell maintenance and organogenesis, despite the absence of WUS-mediated stem cell organization. Our previous work showed that the stem cell-delimiting function of the CLV pathway receptors CLAVATA1 (CLV1) and RECEPTOR-LIKE PROTEIN KINASE2 (RPK2) is conserved in the moss P. patens. Here, we use P. patens to assess whether CLV-cytokinin crosstalk is also an evolutionarily conserved feature of stem cell regulation. Genetic analyses reveal that CLV1 and RPK2 regulate SAM proliferation via separate pathways in moss. Surprisingly, cytokinin receptor mutants also form ectopic stem cells in the absence of cytokinin signaling. Through modeling, we identified regulatory network archtectures that recapitulated the stem cell phenotypes of clv1 and rpk2 mutants, cytokinin application, cytokinin receptor mutations, and higher-order combinations of these perturbations. These models predict that CLV1 and RPK2 act through separate pathways wherein CLV1 represses cytokinin-mediated stem cell initiation and RPK2 inhibits this process via a separate, cytokinin-independent pathway. Our analysis suggests that crosstalk between CLV1 and cytokinin signaling is an evolutionarily conserved feature of SAM homeostasis that preceded the role of WUS in stem cell organization.

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“…Similarly, we now show using both hypocotyl grafts between the WT and the cra2 mutant and split-root experiments with CEP7 peptides that the promotion of nodulation induced by MtCEP7 peptides relies on MtCRA2 and that this regulation occurs systemically in distant non-treated roots through the activity of the MtCRA2 receptor in shoots. There is scarce knowledge on how peptide hormone signaling intersects with metabolite hormones, such as cytokinin 51,52 . An example in Arabidopsis is the regulation by WUSCHEL of AtCLV3 expression in the shoot apical meristem, which is itself a direct target of cytokinin signaling 52,53 .…”

Section: Discussionmentioning

confidence: 99%

“…There is scarce knowledge on how peptide hormone signaling intersects with metabolite hormones, such as cytokinin 51,52 . An example in Arabidopsis is the regulation by WUSCHEL of AtCLV3 expression in the shoot apical meristem, which is itself a direct target of cytokinin signaling 52,53 . The M. truncatula model offers a unique opportunity to dissect how two independent systemic signaling pathways regulate symbiotic nodulation antagonistically 36,41 .…”

Section: Discussionmentioning

confidence: 99%

The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically

et al. 2020

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Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. C-terminally Encoded Peptides (CEPs) and CLAVATA3like (CLE) peptides positively and negatively regulate nodulation, respectively, through independent systemic pathways, but how these regulations are coordinated remains unknown. Here, we show that rhizobia, Nod Factors, and cytokinins induce a symbiosisspecific CEP gene, MtCEP7, which positively regulates rhizobial infection. Via grafting and split root studies, we reveal that MtCEP7 increases nodule number systemically through the MtCRA2 receptor. MtCEP7 and MtCLE13 expression in rhizobia-inoculated roots rely on the MtCRE1 cytokinin receptor and on the MtNIN transcription factor. MtNIN binds and transactivates MtCEP7 and MtCLE13, and a NIN Binding Site (NBS) identified within the proximal MtCEP7 promoter is required for its symbiotic activation. Overall, these results demonstrate that a cytokinin-MtCRE1-MtNIN regulatory module coordinates the expression of two antagonistic, symbiosis-related, peptide hormones from different families to fine-tune nodule number.

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Cytokinin and CLE signaling are highly intertwined developmental regulators across tissues and species

Cited by 18 publications

References 82 publications

Growth dynamics of the Arabidopsis fruit is mediated by cell expansion

Growth dynamics of the Arabidopsis fruit is mediated by cell expansion

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically

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