Analysis of 101 nuclear transcriptomes reveals 23 distinct regulons and their relationship to metabolism, chromosomal gene distribution and co-ordination of nuclear and plastid gene expression

Abstract

Post-endosymbiotic evolution of the proto-chloroplast was characterized by gene transfer to the nucleus. Hence, most chloroplast proteins are nuclear-encoded and the regulation of chloroplast functions includes nuclear transcriptional control. The expression profiles of 3292 nuclear Arabidopsis genes, most of them encoding chloroplast proteins, were determined from 101 different conditions and have been deposited at the GEO database ( http://www.ncbi.nlm.nih.gov/geo/) under GSE1160–GSE1260 GSE1160 GSE1161 GSE1162 GSE1163 GSE1164 GSE1165 GSE1166 GSE1167 GSE1168 GSE1169 GSE1170 GSE1171 GSE1172 GSE1173 GSE1174 GSE1175 GSE1176 GSE1177 GSE1178 GSE1179 GSE1180 GSE1181 GSE1182 GSE1183 GSE1184 GSE1185 GSE1186 GSE1187 GSE1188 GSE1189 GSE1190 GSE1191 GSE1192 GSE1193 GSE1194 GSE1195 GSE1196 GSE1197 GSE1198 GSE1199 GSE1200 GSE1201 GSE1202 GSE1203 GSE1204 GSE1205 GSE1206 GSE1207 GSE1208 GSE1209 GSE1210 GSE1211 GSE1212 GSE1213 GSE1214 GSE1215 GSE1216 GSE1217 GSE1218 GSE1219 GSE1220 GSE1221 GSE1222 GSE1223 GSE1224 GSE1225 GSE1226 GSE1227 GSE1228 GSE1229 GSE1230 GSE1231 GSE1232 GSE1233 GSE1234 GSE1235 GSE1236 GSE1237 GSE1238 GSE1239 GSE1240 GSE1241 GSE1242 GSE1243 GSE1244 GSE1245 GSE1246 GSE1247 GSE1248 GSE1249 GSE1250 GSE1251 GSE1252 GSE1253 GSE1254 GSE1255 GSE1256 GSE1257 GSE1258 GSE1259 GSE1260 . The 1590 most-regulated genes fell into 23 distinct groups of co-regulated genes (regulons). Genes of some regulons are not evenly distributed among the five Arabidopsis chromosomes and pairs of adjacent, co-expressed genes exist. Except regulons 1 and 2, regulons are heterogeneous and consist of genes coding for proteins with different subcellular locations or contributing to several biochemical functions. This implies that different organelles and/or metabolic pathways are co-ordinated at the nuclear transcriptional level, and a prototype for this is regulon 12 which contains genes with functions in amino acid and carbohydrate metabolism, as well as genes associated with transport or transcription. The co-expression of nuclear genes coding for subunits of the photosystems or encoding proteins involved in the transcription/translation of plastome genes (particularly ribosome polypeptides) (regulons 1 and 2, respectively) implies the existence of a novel mechanism that co-ordinates plastid and nuclear gene expression and involves nuclear control of plastid ribosome abundance. The co-regulation of genes for photosystem and plastid ribosome proteins escapes a previously described general control of nuclear chloroplast proteins imposed by a transcriptional master switch, highlighting a mode of transcriptional regulation of photosynthesis which is different compared to other chloroplast functions. From the evolutionary standpoint, the results provided indicate that functional integration of the proto-chloroplast into the eukaryotic cell was associated with the establishment of different layers of nuclear transcriptional control.