Slicing across kingdoms: regeneration in plants and animals

Abstract

Multicellular organisms possessing relatively long life spans are subjected to diverse, constant, and often intense intrinsic and extrinsic challenges to their survival. Animal and plant tissues wear out as part of normal physiological functions and can be lost to predators, disease, and injury. Both kingdoms survive this wide variety of insults by strategies that include the maintenance of adult stem cells or the induction of stem cell potential in differentiated cells. Repatterning mechanisms often deploy embryonic genes, but the question remains in both plants and animals whether regeneration invokes embryogenesis, generic patterning mechanisms, or unique circuitry comprised of well-established patterning genes.

Figure 1

Regeneration in Animals and Plants: A Historical Perspective (A) Hydra attached to a small twig with its anterior end pointing down. (B) Regeneration of two pieces of willow suspended in opposite orientations show that polarity is preserved with root and shoot regeneration occurring at the respective bases or apices of the fragments. On the right is a root fragment, also regenerating the corresponding shoots or roots and demonstrating that regenerative capacity is widespread across the anatomy of plants. (C) Regeneration of whole plants from the leaf of the pansy Achimenes haageana. The leaf was removed from a flowering plant and regeneration resulted in roots emerging from the base of the leaf-stalk and flowers emerging near stipules. (Image A from Trembley, 1744; image B from Morgan, 1900 and Vöchting, 1885; image C from Goebel, 1898).

Figure 2. Comparison of Major Aspects of Regeneration in Plants and Animals

Descriptions of the known cellular origins, regenerative structures, and patterning mechanisms are indicated. We include also an experimental method described in animals (overexpression of transcription factors and nuclear transplantation), which allows differentiated cells to assume stem cell attributes. Whether or not these cells can contribute to regeneration of adult tissues after injury remains untested (Takahashi et al., 2007; Wernig et al., 2007).

Figure 3. Plant Meristems and Animal Blastemas

(A) Two of the plant’s indeterminate meristems (root apical meristem, RAM, and shoot apical meristem, SAM, respectively) that can be completely regenerated in adult plants, restoring indeterminate growth. The stem cell niche in the root consists of mitotically less active quiescent center cells (green), which maintain adjacent stem cells (shades of blue) in an undifferentiated state. Cells away from the tip are more differentiated. Differentiating pericycle cells (brown) have been found to give rise to callus, which can in turn recreate the entire root or shoot meristem. The structure of the shoot meristem consists of a group of stem cells in the central zone that lie on top of a group of mitotically active cells that are known to signal and maintain the stem cells, similarly as in root. The largely nonoverlapping domains of CUC2 (blue) and WUS (yellow) are super-imposed on the normal SAM. (B) A progression series highlighting the cellular processes that take place in the formation of an animal blastema. This structure is assembled by the division progeny of either stem cells residing in the pre-existing tissues (planaria) or a combination of both stem cells and dedifferentiation (salamanders). Once formed, the blastema differentiates, patterns, and functionally integrates itself with the older tissue.

Figure 4. Invertebrate and Plant Model Systems for Studying Regeneration

(A) The planarian Schmidtea mediterranea (left) and a regeneration series of the anterior end at ~days 1, 3, and 4 after decapitation. (B) Head regeneration in Hydra after decapitation (top) and from a cell aggregate of cells obtained after dissociation of a Hydra into individual cells (bottom). The signal corresponds to the expression of a Chordin-like gene in this organism. Images reproduced from Rentzsch et al. (2007), Proc. Natl. Acad. Sci. USA 104, 3249–3254. Copyright (2007) National Academy of Sciences, USA. (C) Normally developing Arabidopsis with a basal rosette and a reproductive inflorescence that has arisen from the transition of the SAM to a floral meristem (left). Middle, dedifferentiated cell masses of callus that formed from auxin treatment of tissue cuttings from Arabidopsis and the regeneration of a complete shoot from one such callus (right). Images of the callus and regenerating shoot are courtesy of S.P. Gordon and E.M. Meyerowitz.

Figure 5. Remodeling Pre-existing Structures

A trunk fragment of the land planarian Bipalium is shown undergoing remodeling of pre-existing tissues (see text) and the regeneration of the missing head and tail. The animal is drawn at the same magnification for each of the days illustrated. Note the progressive increase in length and decrease in width of the fragment. These changes result in the regeneration of all the missing structures and ultimately reach the appropriate dimensions relative to the sizes of the newly regenerated head and tail. The table indicates days after amputation and the corresponding change in length to width ratio (L:W) for each specimen pictured. This was accomplished by digitizing the original, drawn-to-scale image after Morgan (1900) and measuring along the midline for length and along the geometric center from lateral edge to lateral edge for width.

Figure 6. Signaling Pathways, Axial Polarity, and Regeneration in Planaria

(A) Schmidtea mediterranea planarians subjected to RNAi targeting the key components of Wnt signaling: the Adenomatous polyposis coli (APC) protein and β-catenin (top panel). Abrogation of β-catenin function in amputated animals results in animals that regenerate heads at both ends of the anteroposterior axis. Conversely, accumulation of β-catenin by abrogating its inhibitor (APC) results in animals that regenerate tails and anterior and posterior ends after amputation. In situ panels with a probe against the central nervous system (pro-hormone convertase) demonstrate the presence or absence of brain in RNAi-treated animals. Images from Gurley et al. (2008), Science 319, 323–327. Reprinted with permission from AAAS. (B) Abrogation of the TGF-β pathway prevents mediolateral regeneration as assayed by a probe (D.21) specific to the animal margin (top panel) and also affects dorso-ventral axis maintenance as evidenced by the generation of an extra pair of photoreceptors in the ventral region of the animal (bottom panel). Images are from Reddien et al. (2007) and are reproduced with the permission of the Company of Biologists. In all cases control refers to unc-22, a gene with a nucleotide sequence not found in planarians. Animals were labeled with antibodies that recognize the photoreceptor neurons (VC-1, anti-Arrestin) and the cephalic ganglia (SYT, anti-Synaptotagmin). Scale bars in (A) are 200 μm and in (B) are 100 μm.

Figure 7. Regeneration in Plants

(A) Confocal images of early stage reorganization of SAM in disorganized callus. Red is chlorophyll autofluorescence. Green is a constitutively expressed membrane-bound YFP marker. At left, the membrane-bound YFP marker highlights the small, tightly packed cells that are forming shoot meristems. At right, a close up of the YFP-expressing cells used for imaging analysis and tracking cell division and organ morphology using confocal imaging. Images courtesy of S.P. Gordon and E.M. Meyerowitz. (B) A graphic display of a simulation of auxin fluxes in the root using auxin transport parameters on the simulated cellular structure of the root (left). The series of panels tracks the simulated ablation of QC and the shift of the maximum concentration (dark purple) away from the tip. Images are from Grieneisen et al. (2007) and are reprinted by permission from Macmillan Publishers Ltd: Nature 449, 1008–1013, copyright 2007. The right panel shows GFP driven by the WOX5 promoter, which specifically marks the QC (panel 1, top small panel, pre-ablation). After ablation, the expression of the WOX5 marker shifts proximally away from the root tip (panel 2, 16 hr post-ablation, panel 3, 2 days post-ablation). At 3 days post-ablation (panel 4), the WOX5 marker re-fines itself to a regenerated QC specified by a newly relocated auxin maxima, in agreement with the simulated shift in auxin concentration. The arrow indicates the position of the original QC. Images are from Xu et al. (2006), Science 311, 385–388. Reprinted with permission from AAAS.