Magnesium Limitation Leads to Transcriptional Down-Tuning of Auxin Synthesis, Transport, and Signaling in the Tomato Root

Abstract

Magnesium (Mg) deficiency is becoming a widespread limiting factor for crop production. How crops adapt to Mg limitation remains largely unclear at the molecular level. Using hydroponic-cultured tomato seedlings, we found that total Mg2+ content significantly decreased by ∼80% under Mg limitation while K+ and Ca2+ concentrations increased. Phylogenetic analysis suggested that Mg transporters (MRS2/MGTs) constitute a previously uncharacterized 3-clade tree in planta with two rounds of asymmetric duplications, providing evolutionary evidence for further molecular investigation. In adaptation to internal Mg deficiency, the expression of six representative MGTs (two in the shoot and four in the root) was up-regulated in Mg-deficient plants. Contradictory to the transcriptional elevation of most of MGTs, Mg limitation resulted in the ∼50% smaller root system. Auxin concentrations particularly decreased by ∼23% in the Mg-deficient root, despite the enhanced accumulation of gibberellin, cytokinin, and ABA. In accordance with such auxin reduction was overall transcriptional down-regulation of thirteen genes controlling auxin biosynthesis (TAR/YUCs), transport (LAXs, PINs), and signaling (IAAs, ARFs). Together, systemic down-tuning of gene expression in the auxin signaling pathway under Mg limitation preconditions a smaller tomato root system, expectedly stimulating MGT transcription for Mg uptake or translocation.

Physiological Essence of Magnesium in Plants and Its Widespread Deficiency in the Farming System of China

“…One of the distinct and earliest responses of plants to MGD is the noticeable shrinkage of the root system and the smaller root-to-shoot dry weight (DW) ratio, as a result of restricted photosynthate transportation from source leaves to sink organs (Cakmak et al, 1994a ; Cakmak and Kirkby, 2008 ; Farhat et al, 2016 ; Ishfaq et al, 2021 ; Jia et al, 2021 ). MGD from the initial growth stage remarkably suppresses dry matter production by 34% in barley (Tränkner et al, 2016 ) and 43% in tomato seedlings (Ishfaq et al, 2021 ), which when sufficiently supplied, Mg improves root biomass by 77% compared to a smaller increase in shoot biomass (59%) (Hauer-Jákli and Tränkner, 2019 ). Disrupted root and shoot growth, and resulting decreases in the root/shoot ratio under MGD has been widely investigated (Cakmak et al, 1994a ; Ding et al, 2006 ; Tewari et al, 2006 ; Mengutay et al, 2013 ; da Silva et al, 2017 ; Chen C. T. et al, 2018 ; Ishfaq et al, 2021 ; Xu et al, 2021 ).…”

“…MGD from the initial growth stage remarkably suppresses dry matter production by 34% in barley (Tränkner et al, 2016 ) and 43% in tomato seedlings (Ishfaq et al, 2021 ), which when sufficiently supplied, Mg improves root biomass by 77% compared to a smaller increase in shoot biomass (59%) (Hauer-Jákli and Tränkner, 2019 ). Disrupted root and shoot growth, and resulting decreases in the root/shoot ratio under MGD has been widely investigated (Cakmak et al, 1994a ; Ding et al, 2006 ; Tewari et al, 2006 ; Mengutay et al, 2013 ; da Silva et al, 2017 ; Chen C. T. et al, 2018 ; Ishfaq et al, 2021 ; Xu et al, 2021 ). MGD hampers energy-requiring steps (i.e., Mg-ATP) for carbohydrate translocation toward the root (Section Impaired Carbohydrate Loading and Outflow for detailed description), leading to over-accumulation of carbohydrates in Mg-deficient leaves and substantial reduction of sucrose transport toward roots (Hermans et al, 2005 ; Koch et al, 2020 ).…”

“…MGD hampers energy-requiring steps (i.e., Mg-ATP) for carbohydrate translocation toward the root (Section Impaired Carbohydrate Loading and Outflow for detailed description), leading to over-accumulation of carbohydrates in Mg-deficient leaves and substantial reduction of sucrose transport toward roots (Hermans et al, 2005 ; Koch et al, 2020 ). Further, down-tuning of auxin accumulation and signaling in Mg-deficient root preconditions a smaller root system (Ishfaq et al, 2021 ). A smaller root system under MGD diminishes the root surface area for resource forage in the soil, which further reduces uptake of other nutrients and increases the risk of multiple environmental stresses (Cakmak and Kirkby, 2008 ).…”

“…Where adequate and low Mg were applied as 1.0 mM and 0.02 mM Mg, respectively, in the nutrient solution. Other details on plant growth have been described elsewhere (Ishfaq et al, 2021 ).…”

“…Various other enzymes such as ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), protein kinases, RNA polymerase, glutathione synthase, adenosine triphosphatases (ATPases), phosphatases, and carboxylases require Mg for activation (Maguire and Cowan, 2002 ; Shaul, 2002 ; Dann Iii et al, 2007 ; Marschner, 2012 ). Moreover, Mg participates in sucrose transport, energy metabolism, N utilization, pollen development and male fertility, stress tolerance, plant-microbe interactions, and other numerous biological processes (Li et al, 2008 ; Chen et al, 2009 ; Xu et al, 2015 ; Chen Z. C. et al, 2018 ; Li D. et al, 2020 ; Ishfaq et al, 2021 ; Tian et al, 2021 ).…”