Loss‐of‐function mutation of the calcium sensor CBL1 increases aluminum sensitivity in Arabidopsis

Abstract

Despite the physiological importance of aluminum (Al) phytotoxicity for plants, it remained unknown if, and how, calcineurin B-like calcium sensors (CBLs) and CBL-interacting protein kinases (CIPKs) are involved in Al resistance. We performed a comparative physiological and whole transcriptome investigation of an Arabidopsis CBL1 mutant (cbl1) and the wild-type (WT). cbl1 plants exudated less Al-chelating malate, accumulated more Al, and displayed a severe root growth reduction in response to Al. Genes involved in metabolism, transport, cell wall modification, transcription and oxidative stress were differentially regulated between the two lines, under both control and Al stress treatments. Exposure to Al resulted in up-regulation of a large set of genes only in WT and not cbl1 shoots, while a different set of genes were down-regulated in cbl1 but not in WT roots. These differences allowed us, for the first time, to define a calcium-regulated/dependent transcriptomic network for Al stress responses. Our analyses reveal not only the fundamental role of CBL1 in the adjustment of central transcriptomic networks involved in maintaining adequate physiological homeostasis processes, but also that a high shoot-root dynamics is required for the proper deployment of Al resistance responses in the root.

Dissection of Root Transcriptional Responses to Low pH, Aluminum Toxicity and Iron Excess Under Pi-Limiting Conditions in Arabidopsis Wild-Type and stop1 Seedlings

“…In the case of molecular processes activated in the Aluminum response gene set ( Figure 4A ), we found that the transcript levels of several proteins with kinase activity are increased by Al stress. The upregulation of genes that code for kinases agrees with previous works reporting the involvement of protein phosphorylation in the response of plants to Al 3+ stress ( Osawa and Matsumoto, 2001 ; Panda and Achary, 2014 ; Ligaba-Osena et al., 2017 ). Among the multiple genes coding for kinases enriched in the Aluminum response we found PROLINE RICH LIKE EXTENSION KINASE 4 ( PERK4 ) whose mutant, perk4 , has reduced sensitivity to abscisic acid (ABA) including reduced inhibition of root growth in response to ABA treatment ( Bai et al., 2009 ).…”

“…CIPK17 has been reported to participate in a signaling module that controls Ca 2+ influx and regulates ABA-signaling during stomatal closure ( Song et al., 2018 ). Moreover, the expression of CALCINEURIN B-LIKE PROTEIN 1 (CBL1) was also induced in response to Al, cbl1 mutants have increased sensitivity to Al 3+ toxicity and have downregulated expression of CIPK17 ( Ligaba-Osena et al., 2017 ). CBL1-CIPK17 have been reported to interact in vivo ( Kolukisaoglu et al., 2004 ).…”

The CBL–CIPK Pathway in Plant Response to Stress Signals

“…The earliest studies on AtCBL1 indicated that it was a multifunctional and important protein. Subsequently, numerous studies have confirmed this hypothesis [97,[125][126][127]. We introduce them in the corresponding section.…”

Genome-wide identification of CBL family and expression analysis of CBLs in response to potassium deficiency in cotton

“…In Arabidopsis , 10 genes ( CBL1-10 ) encoding CBL proteins have been found ( Kolukisaoglu et al, 2004 ). CBL1 and CBL9 were reported to positively regulate the uptake and transport of K + , NO 3 − , NH 4 + , aluminum and iron, and the promotion of stomatal opening ( Li et al, 2006 ; Xu et al, 2006 ; Ho et al, 2009 ; Mao et al, 2016 ; Tian et al, 2016 ; Ligaba-Osena et al, 2017 ; Straub, Ludewig & Neuhäuser, 2017 ). CBL1 and CBL9 also affect abscisic acid (ABA)-induced stomatal closure and ROS signaling ( Pandey et al, 2004 ; Cheong et al, 2007 ; Drerup et al, 2013 ).…”