Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots

Abstract

In waterlogged soil, deficiency of oxygen triggers development of aerenchyma in roots which facilitates gas diffusion between roots and the aerial environment. However, in contrast to other monocots, roots of rice (Oryza sativa L.) constitutively form aerenchyma even in aerobic conditions. The formation of cortical aerenchyma in roots is thought to occur by either lysigeny or schizogeny. Schizogenous aerenchyma is developed without cortical cell death. However, lysigenous gas-spaces are formed as a consequence of senescence of specific cells in primary cortex followed by their death due to autolysis. In the last stage of aerenchyma formation, a 'spoked wheel' arrangement is observed in the cortical region of root. Ultrastructural studies show that cell death is constitutive and no characteristic cell structural differentiation takes place in the dying cells with respect to surrounding cells. Cell collapse initiation occurs in the center of the cortical tissues which are characterized by shorter with radically enlarged diameter. Then, cell death proceeds by acidification of cytoplasm followed by rupturing of plasma membrane, loss of cellular contents and cell wall degradation, while cells nuclei remain intact. Dying cells releases a signal through symplast which initiates cell death in neighboring cells. During early stages, middle lamella-degenerating enzymes are synthesized in the rough endoplasmic reticulum which are transported through dictyosome and discharged through plasmalemma beneath the cell wall. In rice several features of root aerenchyma formation are analogous to a gene regulated developmental process called programmed cell death (PCD), for instance, specific cortical cell death, obligate production of aerenchyma under environmental stresses and early changes in nuclear structure which includes clumping of chromatin, fragmentation, disruption of nuclear membrane and apparent engulfment by the vacuole. These processes are followed by crenulation of plasma membrane, formation of electron-lucent regions in the cytoplasm, tonoplast disintegration, organellar swelling and disruption, loss of cytoplasmic contents, and collapse of cell. Many processes in lysing cells are structural features of apoptosis, but certain characteristics of apoptosis i.e., pycnosis of the nucleus, plasma membrane blebbing, and apoptotic bodies formation are still lacking and thus classified as non-apoptotic PCD. This review article, describes most recent observations alike to PCD involved in aerenchyma formation and their systematic distributions in rice roots.

Keywords: Apoptosis; Cell death; Hypoxia; Lysigeny; Programmed cell death; Regulation; Rice.

Fig. 1

Aerenchyma formation in rice roots under hypoxia. a Cross section of roots that emerged under aerobic conditions (15–20 cm from the root base) showing less aerenchyma. b Cross section of roots that emerged under flooded conitions for 2 weeks (0.5 cm from the root-shoot junction) showing fully developed aerenchyma

Fig. 2

Cross section of a root showing programmed cell death during aerenchyma formation in rice roots. a Spatial distribution of cortical cell expansion during later stages. Arrow indicates the radial and tangential cell diameters. b-c Initiation of PCD and radial expansion during aerenchyma development. Arrows indicate the direction of PCD from centre of cortical tissue towards periphery. d Later stages of aerenchyma development showing outer part of roots contained four cell layers (rhizodermis, exodermis, sclerenchyma and one cortical cell layer). e Condensation of the cytoplasm against the edges of the cortical cell during later stages (arrows). f Membrane degaradation before the collapse of the cells during later stages. co cortical cells, ep epidermis, ex exodermis, scl sclerenchyma, st stele

Fig. 3

Schematic model of programmed cell death during aerenchyma formation in rice roots. Aerenchyma in rice roots form by nonapoptotic lysigeny of cortical cells. Hypoxia induced signalling leads to cell enlargement in the mid cortex, followed by nuclear disruption and engulfment by vacuole. In later stages, tonoplast disruption and distortion of cellular organelles occur, followed by the loss of plasma-membrane integrity. After these events, cells lose contact with neighboring (tangential) cells, and collapse. Once cell collapse begins, the cavity then rapidly expands radially leading to aerenchyma formation