CRF transcription factors in the trade-off between abiotic stress response and plant developmental processes

Abstract

Climate change-induced environmental stress significantly affects crop yield and quality. In response to environmental stressors, plants use defence mechanisms and growth suppression, creating a resource trade-off between the stress response and development. Although stress-responsive genes have been widely engineered to enhance crop stress tolerance, there is still limited understanding of the interplay between stress signalling and plant growth, a research topic that can provide promising targets for crop genetic improvement. This review focuses on Cytokinin Response Factors (CRFs) transcription factor's role in the balance between abiotic stress adaptation and sustained growth. CRFs, known for their involvement in cytokinin signalling and abiotic stress responses, emerge as potential targets for delaying senescence and mitigating yield penalties under abiotic stress conditions. Understanding the molecular mechanisms regulated by CRFs paves the way for decoupling stress responses from growth inhibition, thus allowing the development of crops that can adapt to abiotic stress without compromising development. This review highlights the importance of unravelling CRF-mediated pathways to address the growing need for resilient crops in the face of evolving climatic conditions.

Keywords: CRF transcription factors; abiotic stress response; auxin; cytokinin; development; oxidative stress; photosynthesis; senescence.

FIGURE 1

Graphical model illustrating the complex roles of Cytokinin Response Factors (CRFs) in the trade-off between abiotic stress response and plant developmental processes. Coloured boxes highlight the role of specific CRFs in stress responses (yellow box), CK/IAA hormonal crosstalk (light blue and pink boxes) and senescence (green box). The blue box focuses on the involvement of CRFs in cytokinin homeostasis and signalling. The pink box depicts the regulation of auxin transport exerted by CRFs. Lastly, the green box emphasizes the trade-offs between photosynthesis and senescence regulated by CRFs. This model provides a comprehensive view of the multifaceted roles of CRFs in integrating endogenous and exogenous signals to regulate plant development. YELLOW BOX: Under various stress conditions, specific CRFs are transcriptionally regulated and have a role in regulating the specific stress response (Table 1). OS is a common outcome of various abiotic stress responses. During OS response, ANAC017 is released from the mitochondrial membrane and binds to the promoters of CRF5 and CRF6, activating their transcription. ANAC017 also interacts with PIF4 at the protein level, showing a diurnal expression pattern, and repressing circadian regulators LHY and CCA1. CRF5 is also involved in pathogen resistance. LIGHT BLUE BOX: CKs are perceived by membrane-localized histidine kinase receptors (CHKs) and are transduced through histidine phosphotransferase proteins (HPTs) to activate response regulators (RRs) in the nucleus (Kieber and Schaller, 2014). Type-A RRs act as negative regulators of CKs signalling whereas type-B RRs act as transcription factors and are positive regulators in this pathway. CRF5 represses UGT76C2, responsible for cytokinin N-glucosylation, and CRF6 represses genes responsible for CK signalling (ARR6, ARR9, ARR11), biosynthesis (LOG7), and transport (ABCG14). The CRFs exhibit protein-level interactions with HPT, among themselves in various combinations, and with specific RRs, providing contextual flexibility and response specificity to the CK signalling pathway. CRFs 2, 5, and 6 are transcriptionally activated by CKs in a manner dependent on AHK receptors and specific RRs (ARR1 and ARR12). PINK BOX: AtCRF2 and AtCRF6 positively regulate PIN1 and PIN7, while AtCRF3 acts as a negative regulator. AtCRF2 is also auxin-responsive, downstream of MONOPTEROS/ARF5, and participates in root embryogenesis and shoot formation together with SHOOT MERISTEMLESS (STM). CRF2, 3 and 6 are positive regulators of ovule density, pistil length, and placenta length. CRF9 is a negative regulator of silique and seed development and shoot apical meristem floral transition. CRFs are involved also in other auxin-regulated processes such as hypocotyl elongation and vascular patterning. GREEN BOX: CRF2 is under the epigenetic control of SWI/SNF chromatin remodelling complex. CRF2 is a positive senescence regulator, PDV2 is downstream of CRF2 and promotes chloroplast division. CRF6 positively regulates photosynthetic activity and delays senescence by repressing ARR6, a negative regulator of chlorophyll retention. Conversely, crf1/3/5 knockout lines show reduced expression of the senescence regulator SAG12, increased expression of the photosynthesis regulator CAB1, and an early onset of senescence.