Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence

Abstract

A comparative transcriptome analysis for successive stages of Arabidopsis (Arabidopsis thaliana) developmental leaf senescence (NS), darkening-induced senescence of individual leaves attached to the plant (DIS), and senescence in dark-incubated detached leaves (DET) revealed many novel senescence-associated genes with distinct expression profiles. The three senescence processes share a high number of regulated genes, although the overall number of regulated genes during DIS and DET is about 2 times lower than during NS. Consequently, the number of NS-specific genes is much higher than the number of DIS- or DET-specific genes. The expression profiles of transporters (TPs), receptor-like kinases, autophagy genes, and hormone pathways were analyzed in detail. The Arabidopsis TPs and other integral membrane proteins were systematically reclassified based on the Transporter Classification system. Coordinate activation or inactivation of several genes is observed in some TP families in all three or only in individual senescence types, indicating differences in the genetic programs for remobilization of catabolites. Characteristic senescence type-specific differences were also apparent in the expression profiles of (putative) signaling kinases. For eight hormones, the expression of biosynthesis, metabolism, signaling, and (partially) response genes was investigated. In most pathways, novel senescence-associated genes were identified. The expression profiles of hormone homeostasis and signaling genes reveal additional players in the senescence regulatory network.

Figure 1.

A, Venn diagrams showing the numbers of significantly up-regulated and down-regulated genes that are unique or commonly regulated during NS, DIS, and DET. B, Frequency of regulated genes that are assigned to a functional protein category according to the MAtDB. The number of genes on the array assigned to a category is shown in parentheses beside the category designation. Positive and negative values on the scale indicate the fraction of up- and down-regulated genes, respectively.

Figure 2.

TP families with biased frequencies of significantly up- or down-regulated genes during senescence. Behind the TP family designation as defined in the TC system, the TC family code (in brackets) and the number of genes on the array assigned to this family (in parentheses) are indicated. Positive and negative values on the x axis indicate the fraction of up- and down-regulated genes, respectively.

Figure 3.

RLK families with biased frequencies of significantly up- or down-regulated genes during senescence. Behind the kinase family designations, the number of genes on the array assigned to this family is indicated in parentheses. Positive and negative values on the x axis indicate the fraction of up- and down-regulated genes, respectively.

Figure 4.

Autophagy. The expression profiles of four senescence-associated ATG genes are shown. Additional ATG gene expression profiles are shown in Supplemental Figure 2. The averages of the normalized signal values (see “Materials and Methods”) were plotted against the sampling time points. The time scale of the x axis is not linear and different for the NS, DIS, and DET senescence experiments. For the developmental senescence (NS) curve, the signal ratio between the last sampling time point (75y for 75% yellow surface; see Table I) and the 4-week-old reference sample (4w/0 d) is indicated.

Figure 5.

Cytokinin. The expression profiles of six senescence-associated CK genes are shown. The data were processed as described for Figure 4.

Figure 6.

JA. The expression profiles of four senescence-associated JA genes are shown. Additional JA gene expression profiles are shown in Supplemental Figure 3. The data were processed as described for Figure 4.

Figure 7.

GA and BRs. The expression profiles of four senescence-associated GA (A–D) and two BR genes (E and F) are shown. The data were processed as described for Figure 4.