Alternate Bearing in Citrus: Changes in the Expression of Flowering Control Genes and in Global Gene Expression in ON- versus OFF-Crop Trees

Abstract

Alternate bearing (AB) is the process in fruit trees by which cycles of heavy yield (ON crop) one year are followed by a light yield (OFF crop) the next. Heavy yield usually reduces flowering intensity the following year. Despite its agricultural importance, how the developing crop influences the following year's return bloom and yield is not fully understood. It might be assumed that an ‘AB signal’ is generated in the fruit, or in another organ that senses fruit presence, and moves into the bud to determine its fate—flowering or vegetative growth. The bud then responds to fruit presence by altering regulatory and metabolic pathways. Determining these pathways, and when they are altered, might indicate the nature of this putative AB signal. We studied bud morphology, the expression of flowering control genes, and global gene expression in ON- and OFF-crop buds. In May, shortly after flowering and fruit set, OFF-crop buds were already significantly longer than ON-crop buds. The number of differentially expressed genes was higher in May than at the other tested time points. Processes differentially expressed between ON- and OFF-crop trees included key metabolic and regulatory pathways, such as photosynthesis and secondary metabolism. The expression of genes of trehalose metabolism and flavonoid metabolism was validated by nCounter technology, and the latter was confirmed by metabolomic analysis. Among genes induced in OFF-crop trees was one homologous to SQUAMOSA PROMOTER BINDING-LIKE (SPL), which controls juvenile-to-adult and annual phase transitions, regulated by miR156. The expression pattern of SPL-like, miR156 and other flowering control genes suggested that fruit load affects bud fate, and therefore development and metabolism, a relatively long time before the flowering induction period. Results shed light on some of the metabolic and regulatory processes that are altered in ON and OFF buds.

Regulation of Floral Induction in Citrus

“…In satsuma mandarin, CiFT expression increases during fall and winter, in which period floral induction occurs. This increase results from the expression of CiFT2 which is also induced during fall and winter in murcott mandarin (Citrus reticulate Blanco) (Shalom et al, 2012). In kumquat and trifoliate orange, CiFT expression increases during early summer, in which period evocation of flower organs has been initiated, or just before evocation.…”

“…Recently, changes in gene expression in response to fruit bearing have been reported in 'Murcott' (C. reticulata Blanco) (Shalom et al, 2012) -Fambuena et al, 2011), and satsuma mandarin (Nishikawa et al, 2012). In these genotypes, the levels of CiFT expression seem to be high in light-fruiting "off" trees and low in heavy-fruiting "on" trees during the floral inductive period.…”

The Effect of Fruit Bearing on Low-molecular-weight Metabolites in Stems of Satsuma Mandarin (<i>Citrus unshiu</i> Marc.)

“…The suppression of CiFT expression by fruit bearing indicates that CiFT expression is correlated to alternate bearing. Recent studies have attempted to identify the mechanism of al- ternate bearing through proteomic or transcriptomic analysis (Muñoz-Fambuena et al, 2013a, b;Shalom et al, 2012Shalom et al, , 2014. However, further studies are needed to understand fully the alternate bearing in citrus.…”

“…By contrast, in the off-crop trees, the presence of a smaller amount of sink tissues may lead to the accumulation of sugar phosphates as well as starch in the stem. It has been reported that the expression of some of the genes and proteins involved in the Calvin cycle is up-regulated in off-crop trees (Muñoz-Fambuena et al, 2013b;Shalom et al, 2012). Therefore, it is suggested that fruit bearing affects not only gene expression or protein levels but also the levels of substrates in the Calvin cycle.…”

“…It has been indicated that citrus FLOWERING LOCUS T (CiFT) plays an important role in the flowering of citrus and that fruit bearing suppresses floral induction via the suppression of CiFT expression (Nishikawa, 2013;Nishikawa et al, 2007Nishikawa et al, , 2012. In recent years, transcriptomic and proteomic analyses have been conducted regarding alternate bearing in citrus (Muñoz-Fambuena et al, 2013a, b;Shalom et al, 2012Shalom et al, , 2014. In transcriptomic analysis, it was demonstrated that the expression of genes involved in abscisic acid (ABA) metabolism and auxin polar transport was altered in buds by fruit removal (Shalom et al, 2014).…”