Conservation of fruit dehiscence pathways between Lepidium campestre and Arabidopsis thaliana sheds light on the regulation of INDEHISCENT

Abstract

SUMMARYThe mode of fruit opening is an important agronomic and evolutionary trait that has been studied intensively in the major plant model system Arabidopsis thaliana. Because fruit morphology is highly variable between species, and is also often the target of artificial selection during breeding, it is interesting to investigate whether a change in fruit morphology may alter the developmental pathway leading to fruit opening. Here we have studied fruit development in Lepidium campestre, a Brassicaceae species that forms silicles instead of siliques. Transgenic L. campestre plants with altered expression levels of orthologs of A. thaliana fruit developmental genes (ALCATRAZ, FRUITFULL, INDEHISCENT and SHATTERPROOF1,2) were found to be defective in fruit dehiscence, and anatomical sections revealed similar changes in tissue patterning as found in respective A. thaliana mutants. Gene expression analyses demonstrated a high degree of conservation in gene regulatory circuits, indicating that, despite great differences in fruit morphology, the process of fruit opening remains basically unchanged between species. Interestingly, our data identify ALCATRAZ as a negative regulator of INDEHISCENT in L. campestre. By mutant analysis, we found the same regulatory relationship in A. thaliana also, thereby shedding new light on how ALCATRAZ drives separation layer formation.

Evolution of the fruit endocarp: molecular mechanisms underlying adaptations in seed protection and dispersal strategies

“…The valve margins of dehiscent fruit in Lepidium campestre are very similar to that of Arabidopsis and expression of ALC , IND , SHP1 , and SHP2 was likewise found to be limited to the valve margins (Mummenhoff et al, 2009). Lenser and Theißen (2013) showed that RNAi knock-down or over-expression of IND , ALC , SHP , or FUL resulted in the anticipated indehiscent phenotypes and mimicked those observed in Arabidopsis with only minor differences. The regulatory interactions among these genes in FUL or IND lines were also conserved as ALC was found to be a negative regulator of IND in both L. campestre and Arabidopsis (Lenser and Theißen, 2013).…”

“…Lenser and Theißen (2013) showed that RNAi knock-down or over-expression of IND , ALC , SHP , or FUL resulted in the anticipated indehiscent phenotypes and mimicked those observed in Arabidopsis with only minor differences. The regulatory interactions among these genes in FUL or IND lines were also conserved as ALC was found to be a negative regulator of IND in both L. campestre and Arabidopsis (Lenser and Theißen, 2013). In contrast, gene expression of ALC , IND , SHP1 , and SHP2 was found to be abolished in the tissue corresponding to the valve margins in Lepidium appelianum , a Brassica species that produces an indehiscent fruit lacking the separation layer (Mummenhoff et al, 2009).…”

Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean

“…In eudicots, the loss of fruit dehiscence is a derived morphologically adaptive character in many lineages, but very little is known about the genetic basis underlying the evolution and diversification of such an important trait. In Arabidopsis and its relatives in Brassicaceae, the mutants or natural variants with indehiscent fruit are frequently related to the loss-of-function or loss-of-expression of genes involved in the regulation of cell identity of lignified valve margin and ALs 26,55,56 . In the legume plant Medicago, a coding change in SHP orthologs is recently found to be correlative with the origin of the specialized coiled morphology of the indehiscent fruit, but the exact cellular and genetic basis of such fruit indehiscence is still unknown 57 .…”

Significant increase of oleic acid level in the wild species Lepidium campestre through direct gene silencing

“…The AtTIP-41-like gene was used as the reference gene to which the gene expression of the FAD2 and the FAE1 genes was normalized, since this gene was slightly more stably expressed (Fig. S1) and has been published by Lenser and Theissen (2013) and Muhlhausen et al (2013) as a reliable reference gene in the Lepidium species (Table 1).…”