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Dynamic Function and Regulation of Apoplast in the Plant Body

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Dynamic Function and Regulation of Apoplast in the Plant Body J. Plant Res. 111: 133-148, 1998 Journal of Plant Research (~) by The Botanical Society of Japan 1998 JPR Symposium Dynamic Function and Regulation of Apoplast in the Plant Body Naoki Sakurai Faculty of Integrated Arts and Sciences, Hiroshima University, Higashi Hiroshima, 739 Japan Apoplast is the internal environment of plant. Our body energy. The direction of two flows is reverse. Usually, the posses the intemal environment that consists of blood, two routes are allotted to xylem vessel and sieve tube. lympha, and tissue fluid. Plant cells are also cultivated and A German plant scientist, E. ML~nch (1930) coined the term surrounded by a liquid medium in the apoplast. As well as apoplast. He termed the water path apoplast, and the other various important functions of the internal environment in part symplast. He noticed that not only xylem vessel but our body, apoplast function is also prerequisite for the plant also cell wall space is the water path and recognized them life. There are so far seven distinct functions of apoplast. as a single continuum of transportation system of water, but (1) Growth regulation with apoplastic enzymes by altering ignored the space for gas exchange. In terms of circulation cell-wall properties through degradation, synthesis, orienta- of mass flow in plant body described above, apoplast should tion and cross-linking of supra molecules of cell walls, such include the air space for gas exchange. Therefore, the as cellulose, non-cellulosic polysaccharides, proteins, and description that plant body consists of apoplast and symplast lignin; (2) Skeleton sustained by cellulose microfibrils, lignin is a simple and clear definition of plant body. One main and various types of structural proteins with distinctively high function of apoplast is the transportation of sugar with solar content of hydroxyproline, proline or glycine; (3) Skin to energy, though a burdensome problem whether or not sieve defend symplast from desiccation, pathogens' attack and tube is to be included in apoplast remains. harmful environmental factors, such as ozone and sulfur A French physiologist, C. Bernard (1813---1878), coined two dioxide; (4) Transportation route for not only well-known terms, internal secretion (1859) and internal environment molecules of water, inorganic ions, and sugar, but also plant (1865). He described that internal environment is a true hormones, oligosaccharides and proteins; (5) Homeostasis physiological environment inherent to individual organism, of the internal environment by controlling ionic balance, pH and every external influence can reach living cells only and water content; (6) Adhesion of cell to cell; (7) Gas through this internal field. This idea led to the concept, exchange space of leaf for photosynthesis. The present "homeostasis" raised by an American physiologist, W.B. article reviews the recent 'advances in studies of several Cannon (1871--,1945) in 1932. I would emphasize that apo- aspects of the dynamic function and regulation of apoplast. plast is the internal physiological environment of plant body. Table 1 summarizes the function of apoplast. There are Key. words~ Cell wall--Defense--Fruit ripening-- seven classified functions, though some of them are still Glucanase -- IAA -- Transportation speculative. Molecules that exist in apoplast and play a role in the specified function, are listed in the table as apoplastic molecules. Enzymes involved in the functions Stephen Hales (1677--.1761) tried to find a heart in plant are listed in the next column. Enzymes that are confirmed body. He might have been influenced by Harvey's famous or suggested to be localized to apoplast are marked with theory of blood circulation published in 1628. Hales' con- asterisks. The classification of Table 1 is analogous to that clusion was somehow strange; there were two hearts, one is of our body. We have bones (as endoskeleton), skin, and root and the other leaf. His conclusion, however, includes blood vessel (as transportation route). Our lymphatic system reality. Some plants generate root pressure. Transpiration is fighting against pathogens to recognize invading organ- of water through leaf stomata is definitely the motive force isms by an immune system. Our individual cells are for water movement from soil. Is there circulation system in attached each other by cell-cell adhesion protein such as plant ? Does plant circulate blood ? These might be the transmembrane proteins (cadherins, connexins, integrins, and next questions that Hales wanted to answer. selectins) and extracellular matrix (fibronectin). Our air Plant does not circulate liquid, but water passes through space for gas exchange is, of course, lung. The only plant body in one direction. Carbon dioxide that enters difference between animal and plant for the above classifi- through leaf stomata into internal air space is converted to cation, is the growth regulated by apoplast in plant. The sugar by the aid of photosynthesis. Produced sugar that plant cells extend or expand many folds after cell division, contains solar energy flows down to stem and root. In this while our body essentially grows (extends and expands) by sense, plant has a definitive route for flow of water and solar cell division, except for the fat cells which can expand after 134 N. Sakurai Table 1 Functions of apoplast and related molecules in plants Function Apoplastic molecules Related enzymes Remarks 1. Growth regulation a) Degradative 1, 3 : 1, 4-/~-Glucan 1, 3 : 1, 4-/%Glucanase* Poaceae Xyloglucan 1, 4-~-Glucanase* Dicots Fruit softening Endo-xyloglucan tTansferase* Dicots Callose 1, 3-,8-Glucanase* Pollen tube Expansin ? Dicots Pectin Polygalaoturonase Fruit softening b) Synthetic Cellulose UDPG- pyrophosphorylase Gibbrellin Pectin and callose Transferase (Golgi) Pollen c) Directional Cellulose 1, 4-,8-Glucan synthase Cortical microtubles Gibberellin d) Cessational Xyloglucan Endo-xyloglucan llansferase* Dicots Diferulic acid (DFA) Peroxidase (POX)* 2. Skelton Cellulose Cellulose synthase Secondary wall Lignin, H202, Phenylpropane PAL*, CAD*, POX*, SOD Secondary wall Glycine-rieh proteins Vascular tissues Proline-rich proteins Extensin 3. Skin a) Dessication defence Cutin Lipid tTansfer protein* Epidermis Mucilage Transferase (Golgi) Root b) Pathogen Thionins Pectin (plant) Polygalacturonase* Extracellular 1, 3 : 1, 6-,8-Glucan (pathogen) 1, 3-,8-Glucanasas* Extracellular Chitin (pathogen) Chitinases* Extracellular ATP ? ATPase* Chitin-binding-protein Extensin ? Proline-rich protein (S-glyceproteins) S- RNase* c) Air pollutant Ozone Ascerbic acid Ascerbate peroxidase* Sulfur dioxide Ferulic acid, H202 Peroxidese* 4. Transportation route H20 Inorganic ions Hormone (IAA, Cytokinin) IAAId oxidase* Sugars Invertase* Extracellular Oligosaccharides Hydrolase ? Xylem exudate Oligopeptides Protease ? Xylem exudate Suberin 5. Homeostasisof internal environment a) Ion balance P, CI, K, Ca, B etc Channel Vacuole b) pH H + H+-ATPase Plasma membrane c) Water content Cell walls Cell wall pore Mucilage Transferase (Golgi) Cactus 6. Adhesion (cell to cell) Arabinogalactan Integlin-like protein 7. Air-space CO2, 02 Endo-1, 3 : 1, 4-,8-glucanase* Spongy tissue 8. Unknown Lectin Extensine Glycine-rich proteins Proline-rich proteins Arabinogalaotan proteins PAL phenylalanin ammonialyase; CAD, cinnamyl alcohol dehydrogenase; POX, peroxidase; SOD, superoxide dismutase. Dynamic Function and Regulation of Apoplast ]3_~ cell division even at middle age. In this review, I disucss gene(s) for the above glucanases is still lacking. Recently recent advances of some aspects of the function and regu- Inouhe and Nevins (1997) proposed that the non-enzymatic lation of apoplast listed in Table 1. proteins regulate the activities of wall-bound glucanases in maize coleoptiles. Growth Regulation Two isozymes (El and Ell) of endo-1, 3 : 1, 4-~-glucanases were found in germinated barley grains (Woodward and Growth regulation in the apoplast can be classified into Fincher 1982). Although these isozymes may not be bound four phases; a) stimulation of growth by degradation of non- to cell walls, they certainly function as a apoplastic enzyme cellulosic polysaccharides by auxin action, b) stimulation of on the seed germination to digest the endosperm cell walls, growth by synthesis of cell wall polysaccharides in response which facilitates the access of (z-amylase to endosperm to gibberellin, c) directional regulation of cellulose microfi- starch granules (Fincher 1989). The gene for isoenzyme El brils by gibberellin action, and d) cessation of growth by was also transcribed in young leaves and roots and the forming cross-links among phenylpropanoids, cell wall pro- expression was stimulated by iAA in young leaves but inhib- teins, non-cellulosic polysaccharides and cellulose. ited in young roots (Slakeski and Fincher 1992a), suggesting the involvement of El in the growth regulation. It, however, Growth regulation by degradation of non-cellulosic polysac- is surprising that the gene for El was not expressed in the charides by auxin action coleoptiles (Slakeski and Fincher 1992b). This regulation involves degradative changes in cell wall In most dicots, the target polysaccharides in auxin-in- architecture induced by auxin. In Poaceae, major non- duced elongation growth are xyloglucan. The degradation cellulosic polysaccharides, 1, 3 : 1, 4-/%glucan, are degraded of xyloglucan induced by auxin action has been reported in by the action of auxin, leading to the decrease in viscosity of many dicot
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