Kitin et al.IAWA – Earlywood Journal 37vessel (2), development2016: 315–331 and function 315 EARLYWOOD VESSELS IN RING-POROUS TREES BECOME FUNCTIONAL FOR WATER TRANSPORT AFTER BUD BURST AND BEFORE THE MATURATION OF THE CURRENT-YEAR LEAVES Peter Kitin1, 2,* and Ryo Funada3 1USDA Forest Service, Forest Products Laboratory, One Gifford Pinchot Drive, Madison, WI 53726, U.S.A. 2Madison Area Technical College, 1701 Wright Street, Madison, WI 53704, U.S.A. 3Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu-Tokyo 183-8509, Japan *Corresponding author; e-mail: [email protected] ABSTRACT This paper reviews the development of xylem vessels in ring-porous dicots and the corresponding leaf phenology. Also included are our original observations on the time-course of vessel element growth, secondary wall deposition, and end wall perforation in the deciduous hardwood Kalopanax septemlobus. Dif- ferent patterns of xylem growth and phenology serve different strategies of the species for adaptation to seasonal climates. Trees with ring-porous xylem form wide earlywood vessels (EWV) in spring and narrow latewood vessels in sum- mer. The wide EWV become embolized or blocked with tyloses by the end of the growing season while the narrow vessels may remain functional for many years. The co-occurrence of wide and narrow vessels provides both efficiency and safety of the water transport as well as a potentially longer growing sea- son. It has for a long time been assumed that EWV in ring-porous hardwoods are formed in early spring before bud burst in order to supply sap to growing leaves and shoots. However, the full time-course of development of EWV elements from initia- tion of growth until maturation for water transport has not been adequately studied until recently. Our observations clarify a crucial relationship between leaf maturation and the maturation of earlywood vessels for sap transport. Accumulated new evidence shows that EWV in branches and upper stem parts develop earlier than EWV lower in the stem. The first EWV elements are fully expanded with differentiated secondary walls by the time of bud burst. In lower stem parts, perforations in vessel end walls are formed after bud burst and before the new leaves have achieved full size. Therefore, the current-year EWV network becomes functional for water transport only by the time when the first new leaves are mature. Keywords: Deciduous, earlywood, functional ecology, phenology, ring-porous, tree ring, vessel maturation, xylem formation, Kalopanax. © International Association of Wood Anatomists, 2016 DOI 10.1163/22941932-20160136 Published by Koninklijke Brill NV, Leiden Downloaded from Brill.com10/08/2021 11:24:09PM via free access 316 IAWA Journal 37 (2), 2016 INTRODUCTION Species with ring-porous wood, among them deciduous oaks, ashes, elms, chestnuts, mulberries, and some representatives of the legumes, are wide-spread in temperate climates. Such species form wide earlywood vessels in the beginning of the growing season followed by distinctly smaller latewood vessels later in the growing season. The large earlywood vessels transport sap during the year in which they are formed while the previous-year large vessels are typically blocked with tyloses (Ellmore & Ewers 1986; Utsumi et al. 1999; Umebayashi et al. 2008; Dié et al. 2012; De Micco et al. 2016; García-González et al. 2016). In contrast, the small-diameter latewood con- duits may remain functional for many years similarly to the xylem vessels in diffuse- porous hardwoods such as alder, basswood, birch, poplar and many other temperate or boreal species that lack wide vessels (Umebayashi et al. 2008). Larger vessel diam- eter provides higher capacity for water transport which results in more photosynthetic gain and growth. However, in conditions of drought or winter freezing, large-diameter vessels are vulnerable to embolism and dysfunction (Cochard & Tyree 1990; Sperry et al. 1994; Lo Gullo et al. 1995; Hacke & Sperry 2001; Taneda & Sperry 2008; Beeckman 2016). In contrast, small-diameter vessels are relatively resistant to the environmental factors that cause xylem dysfunction. It is widely agreed among plant physiologists that the simultaneous occurrence of wide and narrow vessels in a single growth ring ensures efficiency of the sap transport in periods of intensive growth and at the same time sustainability of the transport system during unfavorable climatic conditions (Baas 1976; Carlquist 1980). A positive relationship was also found be- tween smaller vessels in latewood and delayed autumn leaf senescence (Yin et al. 2015). Xylem water transport in wide conduits can be affected by decreased precipitation or a sudden drop in temperature and, therefore, smaller vessels might be important for sustaining the growth in autumn. In normal conditions, however, earlywood vessels are filled with water during the autumn shedding of leaves and until the occurrence of the first hard frost (Utsumiet al. 1996, 1999). Cochard and Tyree (1990) summarized the life history of Quercus earlywood vessels with the following sequence of events: growth in early spring; functional water conduction until early fall with a loss of about 20% of water conductivity by August; embolism by the first hard frost in fall; and gradual growth of tyloses until the vessels are completely blocked by the following summer. Ring-porosity and semi-ring porosity are not restricted to temperate species but oc- cur in several tropical species as well such as semi-deciduous teak (Tectona grandis), cedro (Cedrela sp.), Melia azedarach, Grewia damine, Toona sp., Balanites sp., and some Pterocarpus and Dalbergia sp. Alternation of wet and dry seasons may result in formation of xylem rings (Tarelkin et al. 2016) but the factors affecting ring poros- ity in tropical species have not been explicitly investigated. A relationship between the timing of earlywood formation in teak and the pattern of precipitation during the growing season in Ivory Coast was noted by Dié et al. (2012). They observed that earlywood formation occurred in the first 2–3 months of the rainy season coinciding with the highest peak of precipitation. Formation of latewood was initiated prior to Downloaded from Brill.com10/08/2021 11:24:09PM via free access Kitin et al. – Earlywood vessel development and function 317 a short 1–2-month drier period and then a second precipitation peak occurred before the main dry season and the onset of cambial dormancy. In contrast, teak in irrigated young plantations forms diffuse-porous rings with less or no distinction between ear- lywood and latewood (Priya & Bhat 1999). In deciduous and semi-deciduous Cedrela sp., thick-walled latewood fibers and small-diameter vessels were formed during a dry period before leaf senescence (Dünisch et al. 2002; Marcati et al. 2006; Costa et al. 2013). In addition to ring porosity, other intra-annual variations in wood structure may occur which are defined as growth zones by Dié et al. (2012) or false rings by Priya and Bhat (1998). Studies on the cambial activity in tropical species are becoming in- creasingly important for defining the anatomical distinction between annual rings and intra-annual densities (Bräuning et al. 2016). Ring-porous and diffuse-porous deciduous species have distinct patterns of leaf de- velopment which appear related with the growth patterns of shoots and xylem growth rings. Ring-porous species simultaneously produce leaves and wide earlywood vessels during a short period in the beginning of seasonal growth whereas the production of the first vessels in the stem of diffuse-porous species is after the development of the first current-year leaves (Takahashi et al. 2015; Takahashi & Takahashi 2016). The cambial activity, the duration of xylem element formation, and the timing of the growth of leaves are strongly influenced by environmental conditions (Kitin 1990; Fontiet al. 2007; Rossi et al. 2008; Begum et al. 2013) and regulated by supply with auxin (Aloni & Peterson 1997; Sundberg et al. 2000). They also depend on the allocation of stor- age carbohydrate (Michelot et al. 2012; Begum et al. 2013). On the other hand, the morphogenetic events of leaf, shoot and secondary xylem development are those that build the hydraulic system of the tree and we know that a variety of hydraulic archi- tectures co-exist (Dünisch & Moraes 2002; McCulloh et al. 2010). The ring-porous and diffuse-porous types of xylem appear to be governed by different strategies of the species to adapt fluctuating environmental conditions. Spring reactivation of cambium and wood formation in ring-porous hardwoods commence prior to bud break and, because the previous-year earlywood vessels are not functional, it is assumed that the new vessel elements must play a vital role for providing sap transport during the flush of new leaves (Ellmore & Ewers 1986; Suzuki et al. 1996; Utsumi et al. 1996, 1999). In spring, the putative vessel elements undergo rapid enlargement, deposition and lignification of secondary cell wall, and finally cell apoptosis (Wakuta et al. 1973; Buvat 1989). The development of secondary wall continues for some time after the vessel elements have fully expanded. The forma- tion of perforations and the degeneration of cytoplasm are concomitant or occur just before the programmed death of the cells (Yata et al. 1970; Murmanis 1978; Meylan & Butterfield 1981; Butterfield & Meylan 1982). According to Murmanis (1978), the breakdown of end walls is a gradual process brought about by the activity of the vessel elements’ protoplasm. The temporal and structural development of earlywood vessels, however, may vary to some degree within and between species, along the height of individual trees, and from year to year depending on the environmental conditions (Tepper & Hollis 1967; Zasada & Zahner 1969; Fahn & Werker 1990; Kitin 1990; Takahashi & Takahashi Downloaded from Brill.com10/08/2021 11:24:09PM via free access 318 IAWA Journal 37 (2), 2016 2016). There is still no clear understanding of the complex interrelationship between developmental stages of earlywood vessels and leaf phenology and of the extrinsic and intrinsic factors that underly this interrelationship.