Genetic control of compound leaf development in the mungbean (Vigna radiata L.)

Abstract

Many studies suggest that there are distinct regulatory processes controlling compound leaf development in different clades of legumes. Loss of function of the LEAFY (LFY) orthologs results in a reduction of leaf complexity to different degrees in inverted repeat-lacking clade (IRLC) and non-IRLC species. To further understand the role of LFY orthologs and the molecular mechanism in compound leaf development in non-IRLC plants, we studied leaf development in unifoliate leaf (un) mutant, a classical mutant of mungbean ( Vigna radiata L.), which showed a complete conversion of compound leaves into simple leaves. Our analysis revealed that UN encoded the mungbean LFY ortholog (VrLFY) and played a significant role in leaf development. In situ RNA hybridization results showed that STM-like KNOXI genes were expressed in compound leaf primordia in mungbean. Furthermore, increased leaflet number in heptafoliate leaflets1 (hel1) mutants was demonstrated to depend on the function of VrLFY and KNOXI genes in mungbean. Our results suggested that HEL1 is a key factor coordinating distinct processes in the control of compound leaf development in mungbean and its related non-IRLC legumes.

References

[1] Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69 (1996).

[2] Sinha, N. R., Williams, R. E. & Hake, S. Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev. 7, 787-795 (1993).

[3] Jackson, D., Veit, B. & Hake, S. Expression of maize KNOTTED 1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405-413 (1994).

[4] Hareven, D., Gutfinger, T., Parnis, A., Eshed, Y. & Lifschitz, E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84, 735-744 (1996).

[5] Chen, J. J., Janssen, B. J., Williams, A. & Sinha, N. A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 9, 1289-1304 (1997).

[6] Bharathan, G. et al. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296, 1858-1860 (2002).

[7] Hay, A. & Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 38, 942-947 (2006).

[8] Rast-Somssich, M. I. et al. Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta. Genes Dev. 29, 2391-2404 (2015).

[9] Parnis, A. et al. The dominant developmental mutants of tomato, Mouse-ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9, 2143-2158 (1997).

[10] Shani, E. et al. Stage-specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1-LIKE HOMEOBOX proteins. Plant Cell 21, 3078-3092 (2009).

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

[12] Champagne, C. E. et al. Compound leaf development and evolution in the legumes. Plant Cell 19, 3369-3378 (2007).

[13] Zhou, C. et al. STM/BP-like KNOXI is uncoupled from ARP in the regulation of compound leaf development in Medicago truncatula. Plant Cell 26, 1464-1479 (2014).

[14] Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F. & Meyerowitz, E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843-859 (1992).

[15] Hofer, J. et al. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7, 581-587 (1997).

[16] Wang, H. et al. Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol. 146, 1759-1772 (2008).

[17] Taylor, S., Hofer, J. & Murfet, I. Stamina pistilloida, the Pea ortholog of Fim and UFO, is required for normal development of flowers, inflorescences, and leaves. Plant Cell 13, 31-46 (2001).

[18] Chen, J. et al. Control of dissected leaf morphology by a Cys(2)His(2) zinc finger transcription factor in the model legume Medicago truncatula. Proc. Natl Acad. Sci. USA 107, 10754-10759 (2010).

[19] Ge, L. & Chen, R. PHANTASTICA regulates leaf polarity and petiole identity in Medicago truncatula. Plant Signal. Behav. 9, e28121 (2017).

[20] Zhou, C. et al. The transacting short interfering RNA3 pathway and no apical meristem antagonistically regulate leaf margin development and lateral organ separation, as revealed by analysis of an argonaute7/lobed leaflet1 mutant in Medicago truncatula. Plant Cell 25, 4845-4862 (2013).

[21] Peng, J., Berbel, A., Madueño, F. & Chen, R. AUXIN RESPONSE FACTOR3 regulates compound leaf patterning by directly repressing PALMATE-LIKE PENTAFOLIATA1 expression in Medicago truncatula. Front. Plant Sci. 8, 1630 (2017).

[22] Wang, Z. et al. Multiple components are integrated to determine leaf complexity in Lotus japonicus. J. Integr. Plant Biol. 55, 419-433 (2013).

[23] Wang, Y. & Chen, R. Regulation of compound leaf development. Plants 3, 1-17 (2013).

[24] Chen, C., Wang, S. & Huang, H. LEUNIG has multiple functions in gynoecium development in Arabidopsis. Genesis 26, 42-54 (2002).

[25] Luo, J. H. et al. Different expression patterns of duplicated PHANTASTICA-like genes in Lotus japonicus suggest their divergent functions during compound leaf development. Cell Res. 15, 665-677 (2005).

[26] Sairam, R. K., Dharmar, K., Chinnusamy, V. & Meena, R. C. Water logging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). J. Plant. Physiol. 166, 602-616 (2009).

[27] Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).

[28] Audic, S. & Claverie, J. M. The significance of digital gene expression profiles. Genome Res. 7, 986-995 (1997).

[29] Sangsiri, C., Sorajjapinun, W. & Srinivesc, P. Gamma radiation induced mutations in mungbean. ScienceAsia 31, 251-255 (2005).

[30] Kang, Y. J. et al. Genome sequence of mungbean and insights into evolution within Vigna species. Nat. Commun. 5, 443-5451 (2014).

[31] Shim, J. S., Kubota, A. & Imaizumi, T. Circadian clock and photoperiodic flowering in Arabidopsis, CONSTANS is a hub for signal integration. Plant Physiol. 173, 5-15 (2017).

[32] Molinero-Rosales, N. et al. FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20, 685-693 (1999).

[33] Monniaux, M. et al. Conservation vs divergence in LEAFY and APETALA1 functions between Arabidopsis thaliana and Cardamine hirsuta. New Phytol. 216, 549-561 (2017).

[34] Hay, A. et al. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 12, 1557-1565 (2002).

[35] Barkoulas, M., Hay, A., Kougioumoutzi, E. & Tsiantis, M. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat. Genet. 40, 1136-1141 (2008).

[36] Magnani, E. & Hake, S. KNOX lost the OX, The Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20, 875-887 (2008).

[37] Kimura, S., Koenig, D., Kang, J., Yoong, F. Y. & Sinha, N. Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr. Biol. 18, 672-677 (2008).

[38] Blakeslee, A. F. A unifoliolate mutation in adzuki bean. J. Hered. 4, 153-155 (1919).

[39] Rawal, K. M., Porter, W. M., Franckowiak, J. D., Fawole, I. & Rachie, K. O. Unifoliolate leaf, A mutant in cowpeas. J. Hered. 67, 193-194 (1976).

[40] Moyroud, E. et al. Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor. Plant Cell 23, 1293-1306 (2011).

[41] Winter, C. M. et al. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell. 20, 430-443 (2011).

[42] Yamaguchi, N., Yamaguchi, A., Abe, M., Wagner, D. & Komeda, Y. LEAFY controls Arabidopsis pedicel length and orientation by affecting adaxial-abaxial cell fate. Plant J. 69, 844-856 (2012).

[43] Di Giacomo, E. et al. KNAT3/4/5-like class 2 KNOX transcription factors are involved in Medicago truncatula symbiotic nodule organ development. New Phytol. 213, 822-837 (2017).

[44] Peng, J. et al. Regulation of compound leaf development in Medicago truncatula by fused compoundleaf1, a class M KNOX gene. Plant Cell 23, 3929-3943 (2011).

[45] Tadege, M. et al. Large scale insertional mutagenesis using Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 54, 335-347 (2008).

[46] Małolepszy, A. et al. The LORE1 insertion mutant resource. Plant J. 88, 306-317 (2016).

[47] Li, Z. et al. Development and utilization of a new chemically-induced soybean library with a high mutation density. J. Integr. Plant Biol. 59, 60-74 (2017).

[48] Fehr, W. R. Genetic control of leaflet number in soybeans. Crop Sci. 12, 221-224 (1972).

[49] Fawole, I. Genetic control of leaflet number and shape in cowpea, Vigna unguiculata (L) Walp.. Niger. J. Sci. 34, 73-80 (2000).

[50] Seversike, T. M., Ray, J. D., Shultz, J. L. & Purcell, L. C. Soybean molecular linkage group B1 corresponds to classical linkage group 16 based on map location of the lf (2) gene. Theor. Appl. Genet. 117, 143-147 (2008).