Cell Fate and Cell Morphogenesis in Higher Plants
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Cell fate and cell morphogenesis in higher plants John W Schiefelbein University of Michigan, Ann Arbor, USA The differentiation of plant cells depends on the regulation of cell fate and cell morphogenesis. Recent studies have led to the identification of mutants and the cloning of genes that influence these processes. In several instances, the genes encode products with homeodomains or Myb or Myc DNA-binding domains. Current Opinion in Genetics and Development 1994, 4:647451 Introduction mutants led eo the early notion that iUVl influences the Gte of leaf cells. Recent studies have shed light on the In higher plants, the formation and differentiation of normaI role of KNY. In localization experiments, KNl cells occurs in an orderly manner, ofien near meristems, is undetectable in leaves, but it is abundant in the api- which are groups of dividing cells chat act like permanent cal meristem and the immature axes of vegetative and stem cell populations. Cell differentiation in plants dif- floral shoots [7]. Also, the dominant Knl-N2 mutation fers horn that in animals because, for the most part, of a has been found to cause ectopic expression, such that lack of the relative cell movements that are characteristic KZVZ transcripts and KNl protein are detected in lateral of animal development. Also, the rigid plant cell wall veins of developing leaves (in addition to the normal makes the control of cell shape a critical aspect of cell accumulation in the meristem), which correlates well differentiation in plants. with the alterations in leaf cell fite and knot forma- The fate of undifferentiated plant cells is influenced pri- tion associated with Krzl mutants [7]. When the KNY marily by cell position rather than cell lineage [1,2]. cDNA is expressed in tobacco under the control of the Thus, one of the current goals in studies of plant cell strong cauliflower mosaic virus (G&IV) 35s promoter, differentiation is to determine how cells acquire and the plants display a reduction in shoot stature with rum- respond to positional cues during development. An- pled or lobed leaves and (in some plants) a loss of apical other goal is to understand how, once a particular &te dominance and severe dwarfism with meristematic tis- is adopted, cell morphogenesis is regulated to generate a sue forming in inappropriate places [8’]. These results cell of the appropriate shape. The application of molec- indicate that the KNl product is associated with inde- ular genetic approaches have led recently to an under- terminate growth and cell divisions, although the lack standing of some of the genes that participate in cell fite of recessive (loss-of-fimction) alleles of KN? prevents a specification or cell morphogenesis in plants. This review complete understanding of the role of this gene. will principally focus on these recent molecular and ge- In addition to the Kn 1 mutations, other dominant maize netic experiments, including a summary of the rapidly mutations affect leaf cell fate, including mutations of growing number of homeobox genes that influence plant the Rough sheath1 (RSl) and Liguleless (Lg3 and Lg4) cell development and some of rhe model systems that are genes [9]. A detailed examination of the Rsl-0 mu- being used to study cell fate and morphogenesis in plants. tant has shown that it is similar to Knl mutants; each possessesdominant neomorphic mutations that act non cell autonomously to cause a transformation ofblade tis- sue to sheath, although the Rsl mutant differs in that it Maize homeobox genes associated with cell fate affects the entire lateral dimension of the ligular region of the leaf, causes affected tissue to display attributes of The homeodomain is an approximately 60 amino acid both sheath and auricle, and does not show a dose re- DNA-binding domain found in a superfamily of eukary- sponse [ 10.1. Although the normal role of RS 1 cannot be otic proteins, some of which regulate cell fate [3,4]. The determined directly by analyzing the neomorphic mu- first plant homeobox gene to be isolated, KNOTTED1 tant phenotype, the RSl gene has recently been found (ml), is associated with dominant neomorphic mu- to encode a KNl-like homeodomain protein (P Becraft, tations that alter leaf development in maize and cause M Freeling, unpublished data cited in [9,10*]). Coinci- excess cell proliferation (knots) along lateral veins of the dentally, the RSI gene was one of several maize home- leaf blade ([S]; reviewed in [6]). The phenotype of Kn 1 obox genes cloned by members of the Hake laboratory Abbreviations CaMV-cauliflower mosaic virus; Cll-GLABRAI; KNl-KNOlTEDl; RSl-Rough sheathl; TTGTRANSPARENT TESTA-GLABRA. 0 Current Biology Ltd 0959-437X 647 648 Diffkentiation and gene regulation [5,11”] by virtue of their sequence similarity to KM. has an amino-terminal region similar to metal-binding The expression of four of these maize hotneobox genes domains (denoted the PHD-finger), but no direct ev- (HVI, RSI, KNOX3, and KZYOX8) has been examined idence for a role in plant development has (yet) been in detail, and in wild-type plants, transcripts 6om each obtained [18]. gene have been shown to accumulate in shoot meris- terns and the developing stem, but not in determinate lateral organs such as leaves or floral organs, nor in root meristems [ll”]. Overall, the pattern of expres- Control of epidermal cell fate in Arabidopsis sion of KNOX8 is similar to that of KM, whereas the RSY and KNOX3 genes are expressed in only a subset The formation of hair-bearing and hairless cells in the of KM-expre&g cells. The expression of these four shoot and root epidermis of Ambidopsis provides a useful genes in the vegetative shoot apical meristem appears to model for the study of cell fate specification. In the shoot predict the site of leaf initiation, as well as portions of epidermis, some of the cells differentiate into trichomes the segmentation unit of the shoot (‘phytomer’) [ll*.]. (leaf hairs), and genetic studies have shown that two The distinct regions of homeobox gene expression are loci, GLM3RA 1 (GL1) and TRANSPARENT TESTA- suggestive of roles for the gene products in defining re- GJYBRA (7TG). are required for the specification of a gional identities within the meristem which influence trichome cell. The CL1 gene encodes a product with the fate of differentiating cells. similarity to the DNA-binding domain of the my6 fam- ily of transcriptional regulators [19], and it appears to act locally in trichome precursor cells, as evidenced by in situ RNA hybridization [20’] and genetic mosaic anal- yses [21*]. Interestingly, two pieces of evidence indicate Cloned homeobox genes associated with that GL1 is not only required for specifying cell fate, developmental abnormalities but also to maintain trichome cell differentiation. First, a weak allele of the g/Y gene @l-2) which is associated The role of plant homeobox genes in cell differentiation with the loss of 27 amino acids from the carboxyl termi- has also been studied in other plant species. A KM-like nus of the protein generates a small number of trichomes, homeobox gene isolated from rice (OSH1) produces al- with some aborted trichomes that cease expanding be- terations in leaf morphology reminiscent of those in Kn 7 fore reaching full size [22]. Second, CL7 transcripts per- mutants when introduced (in multiple copies) into rice sist in the differentiating trichome cells after expression [12-l. When the OSHl cDNA is expressed in Arabidopsis in the surrounding leaf primordia has decreased [20*]. (under CaMV35S control) or tobacco (under the con- These results imply that CL1 may be needed to maintain trol of various promoters), plant morphology is altered the expression of genes involved in cell morphogenesis. dramatically, with abnormalities in shoots, leaves, and flowers, and the formation of excess meristematic tis- The other gene required for trichome cell specification, sue [12*,13]. The OSH? gene appears normally to be TT%, may encode or activate a homolog of the maize R expressed in vegetative shoot apices [12’] which, when gene product [23]. Trichome (and anthocyanin) produc- taken together with the cDNA data, implies that it (like tion is restored to rg mutant plants when a cDNA from KIV7) may be a regulator of cell differentiation in/near the Lc gene of the maize R fhily is introduced under the shoot meristem. the control of the CaMV35S promoter [23]. The R gene family members encode proteins with a basic domain Using reduced-stringency DNA hybridization, a large containing a helix-loop-helix (HLH) motif, similar to number of homeobox genes have been identified that found in the myc class of DNA-binding proteins, from Arubidopsis, and one subf&nily has been shown and an acidic domain characteristic of transcriptional to be characterized by a leucine zipper motif adja- activators [24,25]. In maize, the myc-related R gene cent to the homeodomain (denoted HD-Zip proteins) product and the myb-related C7 product are required [14-163. One HD-Zip gene, HAT4, may play a gen- to activate transcription of genes encoding flavonoid eral role in plant development. Its transcripts accumu- biosynthetic enzymes (reviewed in [26]). Thus, an at- late in all tissues examined, with highest levels in stems tractive possibility is that the TTG gene may encode and leaves [17-l. Transgenic plants expressing an anti- a myc-related product that interacts with the myb-re- sense CaMV35!&h!AT4 gene construct display a gen- lated CL1 to activate trichome cell differentiation in eral delay in development, whereas plants expressing a the developing shoot epidermis. The 7TG gene may Cah4V35s-HAT4 sense construct are tall and develop also play a role in trichome spacing, as the R-express- rapidly [17’].