Delayed greening in phosphorus-efficient Hakea prostrata (Proteaceae) is a photoprotective and nutrient-saving strategy

Hakea prostrata R.Br. (Proteaceae) shows a ‘delayed greening’ strategy of leaf development characterised by reddish young leaves that become green as they mature. This trait may contribute to efficient use of phosphorus (P) during leaf development by first investing P in the development of leaf structure followed by maturation of the photosynthetic machinery. In this study, we investigated the properties of delayed greening in a highly P-efficient species to enhance our understanding of the ecological significance of this trait as a nutrient-saving and photoprotective strategy. In glasshouse-grown plants, we assessed foliar pigments, fatty acids and nutrient composition across five leaf developmental stages. Young leaves had higher concentrations of anthocyanin, P, nitrogen (N), copper (Cu), xanthophyll-cycle pigments and saturated fatty acids than mature leaves. As leaves developed, the concentration of anthocyanins decreased, whereas that of chlorophyll and the double bond index of fatty acids increased. In mature leaves, ~60% of the fatty acids was α-linolenic acid (C18:3 n-3). Mature leaves also had higher concentrations of aluminium (Al), calcium (Ca) and manganese (Mn) than young leaves. We conclude that delayed greening in H. prostrata is a strategy that saves P as well as N and Cu through sequential allocation of these resources, first to cell production and structural development, and then to supplement chloroplast development. This strategy also protects young leaves against photodamage and oxidative stress during leaf expansion under high-light conditions.

Developmental stages of delayed-greening leaves inferred from measurements of chlorophyll content and leaf growth

Chlorophyll (Chl) accumulation and leaf growth were analysed in delayed-greening leaves of Theobroma cacao (L.) to examine whether these parameters are correlated during leaf development and can be used as non-destructive indicators of leaf developmental stages. There was a clear correlation between Chl content and leaf relative growth rate (RGR) and between Chl content and percentage of full leaf expansion (%FLE) under different growth conditions. Five distinct developmental phases were defined according to the correlation between these parameters and corroborated by data from the analyses of leaf growth (epidermal cell size and specific leaf area) or photosynthetic properties (maximal PSII efficiency, CO2 assimilation and non-structural carbohydrate contents). The five phases were characterised by rapid leaf expansion by cell division (I), pronounced cell expansion (II), development of photosynthetic capacity concomitant with reinforcement of leaf structure (III), and maturation (IV and V). The transition from cell division to cell expansion happened uniformly across the leaf lamina between phase I and II; the sink-to-source transition was found between phase III and IV. These results demonstrate coordinated development of photosynthetic machinery and leaf structure in delayed-greening leaves and provide a simple and non-invasive method for estimation of leaf developmental stages in T. cacao.