Intracellular Ca2+ and K+ concentration in Brassica oleracea leaf induces differential expression of transporter and stress-related genes

Abstract

BackgroundOne of the most important members of the genus Brassica, cabbage, requires a relatively high level of calcium for normal growth (Plant Cell Environ 7: 397–405, 1984; Plant Physiol 60: 854–856, 1977). Localized Ca2+ deficiency in cabbage leaves causes tip-burn, bringing about serious economic losses (Euphytica 9:203–208, 1960; Ann Bot 43:363–372, 1979; Sci Hortic 14:131–138, 1981). Although it has been known that the occurrence of tip-burn is related to Ca2+ deficiency, there is limited information on the underlying mechanisms of tip-burn or the relationship between Ca2+ and tip-burn incidence. To obtain more information on the genetic control of tip-burn symptoms, we focused on the identification of genes differentially expressed in response to increasing intracellular Ca2+ and K+ concentrations in B. oleracea lines derived from tip-burn susceptible, tip-burn resistant cabbages (B. oleracea var. capitata), and kale (B. oleracea var. acephala).ResultsWe compared the levels of major macronutrient cations, including Ca2+ and K+, in three leaf segments, the leaf apex (LA), middle of leaf (LM), and leaf base (LB), of tip-burn susceptible, tip-burn resistant cabbages, and kale. Ca2+ and K+ concentrations were highest in kale, followed by tip-burn resistant and then tip-burn susceptible cabbages. These cations generally accumulated to a greater extent in the LB than in the LA. Transcriptome analysis identified 58,096 loci as putative non-redundant genes in the three leaf segments of the three B. oleracea lines and showed significant changes in expression of 27,876 loci based on Ca2+ and K+ levels. Among these, 1844 loci were identified as tip-burn related phenotype-specific genes. Tip-burn resistant cabbage and kale-specific genes were largely related to stress and transport activity based on GO annotation. Tip-burn resistant cabbage and kale plants showed phenotypes clearly indicative of heat-shock, freezing, and drought stress tolerance compared to tip-burn susceptible cabbages, demonstrating a correlation between intracellular Ca2+ and K+ concentrations and tolerance of abiotic stress with differential gene expression. We selected 165 genes that were up- or down-regulated in response to increasing Ca2+ and K+ concentrations in the three leaf segments of the three plant lines. Gene ontology enrichment analysis indicated that these genes participated in regulatory metabolic processes or stress responses.ConclusionsOur results indicate that the genes involved in regulatory metabolic processes or stress responses were differentially expressed in response to increasing Ca2+ and K+ concentrations in the B. oleracea leaf. Our transcriptome data and the genes identified may serve as a starting point for understanding the mechanisms underlying essential macronutrient deficiencies in plants, as well as the features of tip-burn in cabbage and other Brassica species.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2512-x) contains supplementary material, which is available to ...

The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants

“…The leaf edges of cabbage, lettuce and brussels sprouts experiencing Ca deficiency are likely to develop necrotic edges, called tipburn. Lee et al (2016) demonstrated that the relationship between intracellular Ca concentration and tipburn in Brassica oleracea differed between genotypes and were correlated with differential expression of a number of transporter and stress response genes. In apple, Ca deficiency is called bitter bit, reflecting that the fruit skin develop pits and that brown spots appear on the skin and/or in flesh, resulting in a bitter taste (Buti et al, 2018;Yu XM et al, 2018).…”

Transcriptome-Wide Identification and Characterization of Circular RNAs in Leaves of Chinese Cabbage (Brassica rapa L. ssp. pekinensis) in Response to Calcium Deficiency-Induced Tip-burn

“…The ECA pumps (ECA1, ECA3 and ECA4) in endomembranes are essential for the balance of Ca 2+ /Mn 2+ between the cytoplasm and the ER, which serves as a central coordinator of plant development and adaptation to stress 24–26 . Additionally, the expression of Ca 2+ -metabolism-related genes including CAX1 , ACA4 , and ACA11 responds differently to abiotic stresses in different tip-burn-resistant Brassica oleracea 27,28 . These results indicated that ACA, CAX, and ECA transporters participate in the process of Ca 2+ deficiency-induced tip-burn.…”

Identification of the Causative Genes of Calcium Deficiency Disorders in Horticulture Crops: A Systematic Review

“…Lee et al conducted two studies investigating causative genes of tipburn in cabbage [34,35]. In 2013, the authors investigated the expression of Ca 2+ transporter genes in tipburn-susceptible and tipburn-resistant lines [34].…”

“…However, clear relevance of the expression of these genes and Ca 2+ concentration in vacuoles was not observed. In 2016, the same authors conducted RNA-seq (RNA sequencing) using tipburn-susceptible cabbage, tipburnresistant cabbage, and kale samples, from which they identified 1844 loci as tipburn-related phenotype-specific genes [35]. Of these, 16 were specific to tipburn-susceptible cabbage, while 747 were specific to tipburn-resistant cabbage.…”

“…To determine the role of gene expression in the occurrence of Ca deficiency disorders and/or Ca accumulation, 37 articles were reviewed in detail (Tables 1 and 2 and Figures 1 and 2). Twenty-six of the thirty-seven reports showed an association between Ca deficiency and/or Ca accumulation and the expression of Ca 2+ -movement-related genes (Ca 2+ antiporters [27,29,32,35,36,39,[42][43][44][45][46][47][48][49][50]53], calreticulin [30,[51][52][53], Ca 2+ -ATPase [35,36,39,54,55], Ca 2+ channels [55][56][57][58], and PME [35,59]). Of the remaining studies, five studies identified QTLs that described variation in tipburn incidence [25,26,33,34,38].…”