The MutantcrispaReveals Multiple Roles forPHANTASTICAin Pea Compound Leaf Development

Abstract

Pinnate compound leaves have laminae called leaflets distributed at intervals along an axis, the rachis, whereas simple leaves have a single lamina. In simple-and compound-leaved species, the PHANTASTICA (PHAN) gene is required for lamina formation. Antirrhinum majus mutants lacking a functional gene develop abaxialized, bladeless adult leaves. Transgenic downregulation of PHAN in the compound tomato (Solanum lycopersicum) leaf results in an abaxialized rachis without leaflets. The extent of PHAN gene expression was found to be correlated with leaf morphology in diverse compound-leaved species; pinnate leaves had a complete adaxial domain of PHAN gene expression, and peltate leaves had a diminished domain. These previous studies predict the form of a compound-leaved phan mutant to be either peltate or an abaxialized rachis. Here, we characterize crispa, a phan mutant in pea (Pisum sativum), and find that the compound leaf remains pinnate, with individual leaflets abaxialized, rather than the whole leaf. The mutant develops ectopic stipules on the petiole-rachis axis, which are associated with ectopic class 1 KNOTTED1-like homeobox (KNOX) gene expression, showing that the interaction between CRISPA and the KNOX gene PISUM SATIVUM KNOTTED2 specifies stipule boundaries. KNOX and CRISPA gene expression patterns indicate that the mechanism of pea leaf initiation is more like Arabidopsis thaliana than tomato.

Different expression patterns of duplicated PHANTASTICA-like genes in Lotus japonicus suggest their divergent functions during compound leaf development

“…However, some differences were found: the signal for LjKN1 was always stronger and in much restricted area near the central zone of SAM, but the one for LjKN3 was generally weaker and more dispersed. No LjKN1 and LjKN3 transcripts were detected in the compound leaf primordia or leaflet primordia at any stage, consistent with previous reports about no expression of KNOXI genes in the compound leaf primordia in pea [24,30]. On the other hand, we failed to detect the expression of LjKN2 in any tissues at both vegetative and reproductive stages by RNA in situ hybridization.…”

“…Previous studies showed PHAN-KNOXI interaction in pea is similar to that in Arabidopsis [30]. To investigate whether it is the same case in L. japonicus, we isolated KNOXI genes and examined their expression patterns by RNA in situ hybridization.…”

“…STP, an ortholog of UNUSUAL FLORAL ORGANS involved in floral development, also regulates the complexity of compound leaves in pea [29]. CRISPA (CRI), the pea ortholog of PHAN, is believed to be required for adaxialabaxial polarity of leaflets and suppress expression of KNOXI genes in compound leaf primordia in pea [30]. The relation between CRI and KNOXI is similar to that in Arabidopsis, indicating that mechanism controlling pea compound leaves is different from that in tomato.…”

“…The relation between CRI and KNOXI is similar to that in Arabidopsis, indicating that mechanism controlling pea compound leaves is different from that in tomato. However, compound leaves in pea are highly specialized because their lateral organs show distinct identities: stipules, leaflets and tendrils [30], and this raises the question about the function of PHAN-like genes and their interaction with KNOXI genes in other papilionoid legumes with relatively simple form of compound leaf.…”

KNOX genes: versatile regulators of plant development and diversity

“…rs2 encodes a myb-type protein that represses KNOX expression in the lateral organs of several plant species with both simple leaves (such as maize, Arabidopsis and snapdragon) and compound leaves (such as pea and the Arabidopsis relative C. hirsuta). Collectively, these are called ARP proteins [ASYMMETRIC LEAVES1 (AS1) in Arabidopsis, Rough sheath2 in maize, PHANTASTICA in snapdragon] (Byrne et al, 2000;Hay and Tsiantis, 2006;Tattersall et al, 2005;Timmermans et al, 1999;Tsiantis et al, 1999). In these plants, ARP and KNOX gene expression distinguishes leaf founder cell from meristem cell fate in the shoot apex.…”