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Evolution of Compound Leaf Development in Legumes: Evidence for Overlapping Roles of KNOX1 and FLO/LFY Genes

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Plant leaves exist in a dizzying array of shapes and sizes, from the tiny duckweed (Lemna minor) to the enormous Raphia palm (Raphia farinifera), and the simple-leaved poplar (Populus sp) to the deeply lobed oak (Quercus spp) or the delicate compound-leaved Mimosa spp. Class I KNOTTED-like (KNOX1) genes have been found to play an important role in the development of compound leaves in many vascular plants (Bharathan et al., 2002). In simple-leaved plants, such as maize or Arabidopsis, class I KNOX1 genes are expressed in the shoot apical meristem, where they function to maintain indeterminacy. Their expression is repressed in leaf primordia and throughout leaf development, consistent with the determinate growth of these organs. In some cases, ectopic expression in simple leaves results in altered leaf morphology reminiscent of compound leaves (ectopic outgrowths and lobes, and in some cases, ectopic meristems). By contrast, many compound-leaved species show a reactivation of KNOX1 expression during leaf development. Furthermore, overexpression of a KNOX1 homolog in tomato leads to more highly branched compound leaf forms. These observations suggest that compound leaves generally evolve from simple leaves by the induction of KNOX1 genes in the developing leaf, causing leaves to become somewhat shoot like.

In this issue of The Plant Cell, Champagne et al. (pages 3369–3378) show that expression of KNOX1 proteins is associated with compound leaf development in the major subfamilies of legumes (family Fabaceae; see figure ), except for a large subclade known as the inverted repeat–lacking clade (IRLC), which includes fava bean (Vicia), pea (Pisum), and alfalfa (Medicago). Results of further experiments suggest that orthologs of FLORICAULA/LEAFY (FLO/LFY) function in place of KNOX1 genes in the development of compound leaves in the IRLC. The authors hypothesize that overlapping functionality of KNOX1 and FLO/LFY genes in ancestral Fabaceae species enabled the loss of KNOX1 function in compound leaf development in the IRLC.

View larger version (67K): [in this window] [in a new window] [as a PowerPoint slide]   Leaf Form in the Fabaceae. (A) to (D) IRLC members pea (A), wisteria (B), alfalfa (C), and fava bean (D). (E) to (H) Non-IRLC members Cercis (E), soybean (F), Acacia (G), and bean (Phaseolus; [H]).

From a phylogenetic analysis by Wojciechowski et al. (2000), based on plastid matK gene sequences, Cercis (redbud) and Bauhinia were found to be sisters to the rest of Fabaceae. Species in these genera lack complex compound leaves, though they may be bilobed, leading to a question of whether they are truly simple leaves or are simplified from compound-leaved ancestors. Champagne et al. found that KNOX1 protein expression in Cercis occurs both in the SAM and in developing mature leaves. Because this pattern is shared with other more distantly related compound-leaved Fabaceae (excluding members of the IRLC), the authors contend that this supports the hypothesis that the ancestral leaf type was compound and the unifoliolate leaf was derived by a fusion of leaflets.

Given that KNOX1 function in compound leaf development has been lost in the IRLC, what controls formation of compound leaves in members of this clade? It was previously shown that in pea (Pisum sativum), a member of the IRLC, the gene UNIFOLATA (UNI) is required for compound leaf development (Hofer et al., 1997, 2001; Gourlay et al., 2000). UNI is an ortholog of Antirrhinum FLO and Arabidopsis LFY genes, which have a primary function in the regulation of floral meristem initiation in these species. The pea uni mutant exhibits floral abnormalites but also shows a conversion of normally compound leaves into simple leaves. Champagne et al. therefore hypothesize that FLO/LFY has replaced KNOX1 in the regulation of compound leaf development throughout the IRLC.

The authors next undertook a series of interesting experiments to determine whether FLO/LFY genes have the capacity to promote compound leaf development in non-IRLC members and, conversely, whether KNOX1 genes retain the capacity to promote leaf compounding in IRLC members. The first set of experiments involved using RNA interference (RNAi) to silence FLO/LFY orthologs in soybean, a species outside the IRLC. LFY-RNAi–silenced lines showed altered floral development, as expected, and also showed some degree of reduced leaf complexity. Wild-type soybean normally produce a single trifoliate leaf at the second node, whereas the majority of LFY-RNAi–silenced lines produced two opposite simplified leaves (often either unifoliolate or bifoliolate) at the second node. This suggests that FLO/LFY genes have an ancestral role of promoting, albeit slightly, compound leaf development in the legumes. Such a role of FLO/LFY homologs in leaf complexity also appears to be the case in plant species outside the Fabaceae. For example, the FLO/LFY ortholog in tomato, FA, also appears to be a minor determinant of leaf complexity in this species, as described for fa mutants (Molinero-Rosales et al., 1999). The second set of experiments involved overexpressing a KNOX1 gene from the cauliflower mosaic virus 35S promoter in the IRLC species alfalfa. In this case, a number of the transgenic lines produced leaves with more than the usual three leaflets. This suggests that KNOX1 genes retain some capacity for influencing compound leaf development in IRLC species, even though they do not normally fill this role in members of this clade.

These results point to a number of interesting conclusions. First, they suggest that KNOX1 and FLO/LFY genes may have had a degree of overlapping function in ancestral Fabaceae. This explains how the loss of KNOX1 expression in leaves could have occurred without a reversion to simple leaves: as KNOX1 function was lost, the slack was taken up by FLO/LFY in the control of compound leaf development. Second, the data suggest that changes in both regulatory and coding sequences have been important in the evolution of KNOX1 and FLO/LFY genes. There have been alterations in tissue-specific and developmental patterns of KNOX1 gene expression, whereas the additional complexity controlled by FLO/LFY points to shifts in the function of the encoded protein and/or in its targets. Finally, the evidence for overlapping functionality suggests that KNOX1 and FLO/LFY might act through the same or overlapping pathways that promote compound leaf development.

The role of FLO/LFY in vegetative development in Antirrhinum, Arabidopsis, and other angiosperms is poorly understood. These genes appear to function primarily in promoting the transition from vegetative to reproductive development by inducing floral identity genes. Champagne et al. speculate that FLO/LFY acquired new targets and/or interacting partners in IRLC members coincident with coming to play an essential role in compound leaf formation. However, it still retains its ancestral role in establishing floral meristem identity, making this a premier example of a single gene acquiring multiple functions during evolution.

	Footnotes

 
www.plantcell.org/cgi/doi/10.1105/tpc.107.057497

	REFERENCES

TOP REFERENCES

 
Bharathan, G., Goliber, T.E., Moore, C., Kessler, S., Pham, T., and Sinha, N.R. (2002). Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858–1860.[Abstract/Free Full Text]

Champagne, C.E.M., Goliber, T.E., Wojciechowski, M.F., Mei, R.W., Townsley, B.T., Wang, K., Paz, M.M., Geeta, R., and Sinha, N.R. (2007). Compound leaf development and evolution in the legumes. Plant Cell 19: 3369–3378.[Abstract/Free Full Text]

Gourlay, C.W., Hofer, J.M., and Ellis, T.H. (2000). Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, cochleata, afila, and tendril-lessn. Plant Cell 12: 1279–1294.[Abstract/Free Full Text]

Hofer, J., Gourlay, C., Michael, A., and Ellis, T.H. (2001). Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol. Biol. 45: 387–398.[CrossRef][ISI][Medline]

Hofer, J., Turner, L., Hellens, R., Ambrose, M., Matthews, P., Michael, A., and Ellis, N. (1997). UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7: 581–587.[CrossRef][ISI][Medline]

Molinero-Rosales, N., Jamilena, M., Zuira, S., Gomez, P., Capel, J., and Lozano, R. (1999). FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20: 685–693.[CrossRef][ISI][Medline]

Wojciechowski, M.F., Sanderson, M.J., Steele, K.P., and Liston, A. (2000). Molecular phylogeny of the "temperate herbaceous tribes" of papilionoid legumes: A supertree approach. In Advances in Legume Systematics, Part 9, P. Herendeen and A. Bruneau, eds (Kew, UK: Royal Botanical Garden), pp. 277–298.

Related articles in Plant Cell:

Compound Leaf Development and Evolution in the Legumes

Connie E.M. Champagne, Thomas E. Goliber, Martin F. Wojciechowski, Raymond W. Mei, Brad T. Townsley, Kan Wang, Margie M. Paz, R. Geeta, and Neelima R. Sinha
Plant Cell 2007 19: 3369-3378. [Abstract] [Full Text]  

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