IAWA Journal, Vol. 32 (1), 2011: 1–13

The endoparasite ulei ( – ) influences wood structure in three host species of Mimosa

Marina Milanello do Amaral and Gregorio Ceccantini Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, 05508-090 São Paulo - SP, Brazil [E-mail: [email protected]]

SUMMARY Pilostyles species (Apodanthaceae) are endoparasites in stems of the family . The body comprises masses of parenchyma in the host bark and cortex, with sinkers, comprising groups of twisted tracheal elements surrounded by parenchyma that enter the secondary xylem of the host plant. Here we report for the first time the effects of Pilostyles on host secondary xylem. We obtained healthy and parasitized stems from Mimosa foliolosa, M. maguirei and M. setosa and compared vessel element length, fiber length, vessel diameter and vessel frequency, measured through digital imaging. Also, tree height and girth were com- pared between healthy and parasitized M. setosa. When parasitized, plant size, vessel diameter, vessel element length and fiber length are all less than in healthy . Also, vessel frequency is greater and vessels are narrower in parasitized stems. These responses to parasitism are similar to those observed in stressed plants. Thus, hosts respond to the parasite by changing its wood micromorphology in favour of increased hydraulic safety. Key words: Pilostyles, Mimosa, parasitism, xylem, efficiency/safety theory.

INTRODUCTION

Pilostyles Guill. species (Apodanthaceae – Cucurbitales) are holoparasites in stems of the plant family Fabaceae. In this the vegetative body is completely mixed within the host tissues. Body structure is simple, without typical organs such as roots, stems and leaves, but with a system of parenchyma and tracheal elements that invade the host stem. This endophytic system basically comprises masses of parenchyma cells in the host secondary phloem and groups of twisted tracheal elements surrounded by parenchyma cells called sinkers, that penetrate the secondary xylem of the host (Guillemin 1854; Solms-Laubach 1874, 1875; Endriss 1902; Kuijt 1969; Rutherford 1970; Kuijt et al. 1985; Dell et al. 1982; Groppo et al. 2007). The impact of Pilostyles on host secondary vascular tissues has been poorly studied, with only one report of phloem cell damage (Kuijt 1969), which is surprising, given the extensive invasion of the parasite. Flower formation also breaks through the external host tissues, crushing and damaging the phloem in the process. Hemiparasitism, on the

Downloaded from Brill.com09/30/2021 04:29:34PM via free access 2 IAWA Journal, Vol. 32 (1), 2011 other hand, is well studied and its impact on wood of the host is well known . For exam- ple, consequences of hemiparasitism may include any of the following: hemiparasite sinkers push the tracheids aside as they grow (Johnson 1888; Peirce 1905; Heinricher 1921, 1924); parasites may dissolve and absorb ray cells (Peirce 1905); cells may lose both the rigidity of the cell walls and their organization patterns, and tracheids may change in length (Heinricher 1921, 1924; Srivastava & Esau 1961); formation of resin canals, even in plants that normally lack these canals when healthy (Korstian & Long 1922; Heil 1923; Srivastava & Esau 1961); increase in growth ring width (Heil 1923; Heinricher 1924; Cohen 1954; Srivastava & Esau 1961); hypertrophy or fusion of rays through the combining of parasitic tissues and tissues formed as a reaction to parasit- ism (Heil 1923; Srivastava & Esau 1961). Thus, effects of hemiparasitism have been relatively well-documented and analysed, while holoparasitism has been neglected. The impact on the xylem caused by flowering holoparasites is almost unknown, even though the extension of the endophytic system into the center of the host stem has been described. Here we describe in detail the anatomical impact of parasitism by Pilostyles on its host, especially on the secondary xylem.

MATERIALS AND METHODS

Three species of Mimosa parasitized by Pilostyles ulei Solms were studied in two locations (Fig. 1–4): M. maguirei Barneby and M. foliolosa Benth. var. multipinna (Benth.) Barneby at Serra do Cipó (Santana do Riacho – MG: 19° 13' 04" S, 43° 30' 26" W, 1040 m above sea level); and M. setosa Benth. var. paludosa (Benth.) Barneby at the Serra das Almas (Rio de Contas – BA: 13° 31' 14" S, 41° 50' 18" W, 1461 m). Paratized specimens were recognized by the massive flowering on barks. Basal trunk segments (10 cm above the ground) were collected from three healthy and four parasit- ized M. maguirei trees. Segments older than the fifth node were taken from six healthy and eight parasitized of M. foliolosa. Twenty-two individuals (10 healthy, 12 parasitized) of this latter species were also measured (height, basal diameter and circumference). All wood samples and herbarium vouchers of all host/parasite pairs were placed in the collections of the Botany Department at the University of São Paulo (SPF and SPFw). Wood samples from healthy and parasitized plants were macerated following Franklin (1945) and sectioned in a sliding microtome (Leica SM 2000R) to produce transverse, radial longitudinal and tangential longitudinal sections. Samples were stained with safranin, safranin/astra-blue (Johansen 1940; Bukatsch 1972 adapted by Kraus & Arduin 1997) or toluidine-blue (O’Brien et al. 1965). Fresh wood from parasitized and healthy plants were compared with the exposition to phloroglucinol, Steinmetz reactive and ferric chloride (Johansen 1940). For these tests thick sections (50–80 µm) were prepared to enhance response and contrasts. Vessel element length, fiber length, vessel tangential diameter were all measured, and the number of vessels was counted manually using a Zeiss KS1000 microscope. We wished to compare wood of the same age and maturity. To select samples accord- ingly, we took very small samples (every 0.5 mm) from the medulla to the cambium.

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These samples were also macerated following Franklin (1945). Fibers and vessel element lengths were measured. Only mature regions of both parasitized and healthy wood were used, having a minimum diameter of 1.5 cm in M. foliolosa, M. maguirei

Figures 1–4. Specimens of Mimosa foliolosa, M. setosa and M. maguirei parasitized by Pylo- styles ulei. – 1: M. foliolosa bushes. – 2: M. setosa stems, parasitized (P) and non-parasitized (NP). – 3: M. setosa parasitized stem. – 4: P. ulei flower in M. maguirei stem.

Downloaded from Brill.com09/30/2021 04:29:34PM via free access 4 IAWA Journal, Vol. 32 (1), 2011 and M. setosa. Even with such relatively thin trunks, we are sure that the wood was as mature as possible because we sampled the outermost wood in the biggest and thick- est individuals of all known populations and all species have short-living stems (few years). Even without parasites, these trees or stems die naturally when they reach diameters around the values we have sampled. Sections of approximately 80 µm were prepared for confocal microscopic (Zeiss LSM 400) examination. Sections were stained with 1% safranin in 50% ethanol, or with 1% toluidine-blue at 6.8 pH. In this analysis, images were obtained every 2 µm using 488 nm argon-krypton lasers with LP 515 filter (long pass) and 543 nm helium-neon lasers with LP 570 filter. Both images were examined for each sample to better under- stand the three-dimensional structures that the parasite generates in the host (Amaral & Ceccantini in prep.). Wood measurements were compared among healthy and parasitized plants and among species through multivariate analysis of variance (MANOVA). This test allowed us to simultaneously examine differences among species and interactions among responses to parasitism. Statistical results with P < 0.05 were considered significant.

RESULTS

Pilostyles ulei Solms comprises external flowers that seemingly arise from the stem or trunk of the host. Flowers are connected to cellular masses of the endophyte within the extant cortex (if still present), the secondary phloem and the periderm of the host (Fig. 5 & 6). From these endophytic masses, sinkers, that are analogous to roots due to their formation and function, grow towards and within the secondary xylem (Fig. 6–9), bearing tracheal elements (Fig. 7). First, sinkers form a wedge-shape intrusion into the host cambium (Fig. 8) from which they grow into the secondary xylem, often following a ray (Fig. 8 & 9). Endophyte parenchyma masses are never in contact to cambium in early stages of infection. Meristematic cells of parasitic endophyte were observed inside cell masses but never seen in any stage of the sinker development, so it seems likely that the sinkers differentiate from parasite parenchyma cells and its pene- tration in host secondary xylem is not simultaneous to host cambium differentiation and wood formation. Sinkers penetrate de wood radially and disorganize, wrap around or mechanically crush some vessels. A detailed description of Pilostyles ulei vegetative body and the host-parasite connection, including confocal microscopy analysis, will be provided in Amaral & Ceccantini (in prep.). The parasite tissue mass in the host phloem comprises parenchyma or meristem cells, in spherical or ellipsoidal form, interconnected by irregular confluences, in very irregular distribution in the bark (Fig. 10). Near these masses, intercellular spaces may be occupied by individual cells or small groups of cells of the parasite (Fig. 11, indi- cated by arrows). These cells stand out from the rest by virtue of their large nucleus as compared to the host cells. Perforation plates were never seen, so these cells are tracheids (Fig. 12). Wood of these Mimosa spp. is typical of the Mimosoideae (Fig. 13–16) and the spe- cies are indistinguishable by wood anatomy alone. Growth rings are not well defined

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Figures 5–9. Cross sections of Mimosa spp. stems parasitized by Pylostyles ulei. – 5: P. ulei flower development in cortex and secondary tissues of M. foliolosa (safranin /astra-blue). – 6: P. ulei flower fragment connected to sinker in secondary xylem ofM. foliolosa (Steinmetz reaction). – 7: Sinker, composed of tracheids and parenchyma cells, in M. setosa secondary phloem (phloro- glucinol). – 8: Sinker development in M. maguirei cambial zone. – 9: Sinker distal part in M. maguirei secondary xylem (8 and 9 toluidine-blue). – HSP = host secondary phloem; HSX = host secondary xylem; PF = parasite flower; SK = sinker.

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Figures 10–12. Parasitic vegetative body in host wood. – 10: Cell masses of Pylostyles ulei within Mimosa setosa phloem (safranin /astra-blue). – 11: Wavy cell (arrows) of P. ulei in M. maguirei phloem intercellular spaces (toluidine-blue). – 12: Torsion of sinker tracheids in M. foliolosa xylem (confocal montage with multiple cuts and artificial colors on safranin stained sections – scale represents the relative position of structures: red closer from observer and dark- blue more distant). – HP = host phloem; PC = parasite cells. and variable, with only a slight thickening or thinning of the fiber walls and rarely with a marginal parenchyma band. Vessels, from solitary to multiples (2–4), varying in den- sity (averages from 15 to 30 vessels mm-2) and diameter (12–160 µm, averages from 40 to 90 µm). Vessel elements are short, with small tails, and simple perforation plates with bordered rims. The axial parenchyma is vasicentric, aliform, confluent and banded. Intervessel and ray-vessel pitting are alternate and vestured of fairly constant diameter (7 µm on average). Fibers have typically simple to minutely bordered pits (< 3 µm). Rays are uniseriate and biseriate and comprise only procumbent cells or procumbent

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Figures 13–18. Comparison between parasitized and healthy stems. – 13 &14: Cross sections of Mimosa foliolosa xylem, healthy (13) and parasitized (14) (safranin/astra-blue). – 15 & 16: Tangential sections of M. setosa xylem, healthy (15) and parasitized (16) (safranin). – 17 &18: Thick cross sections (50–80 µm) of M. setosa xylem, healthy (17) and parasitized (18); phenolic compounds colored in brown (ferric chloride).

Downloaded from Brill.com09/30/2021 04:29:34PM via free access 8 IAWA Journal, Vol. 32 (1), 2011 and square or upright marginal cells. Vessel-ray pitting is bordered, similar to the inter- vascular pits. At first glance, parasitized wood is slightly different from healthy wood, such as in the quantity of phenolic compounds in the axial and ray parenchyma cells (Fig. 17 & 18).

Table 1. T-test results for healthy or parasitized (by Pylostyles ulei) stems of Mimosa folio- losa, M. maguirei and M. setosa. Pairs of values in italics are the only comparisons that are not different at p < 0.05.

Healthy Parasitized Vessel frequency (mm2) M. foliolosa 24.7 30.4 M. maguirei 8.7 13.7 M. setosa 16.1 19.3

Vessel tangential diameter (µm) M. foliolosa 56.9 43.1 M. maguirei 85.7 48.2 M. setosa 68.3 65.2

Vessel element length (µm) M. foliolosa 273 232 M. maguirei 286 188 M. setosa 254 253

Fiber length (µm) M. foliolosa 689 573 M. maguirei 615 534 M. setosa 529 535

In M. setosa, healthy plants were larger than parasitized plants in both height (176 cm versus 113 cm) and circumference (7.7 cm versus 5.8 cm) (p < 0.05). In M. fo- liolosa and M. maguirei, vessels were wider and fewer in healthy plants. Fibers and vessel elements were shorter only in parasitized M. foliolosa (Table 1). To eliminate pseudoreplication and attend to the assumptions of MANOVA, we log-transformed the wood anatomical variables, then averaged them by individual plant, and then ap- plied the MANOVA to these log transformed averages. Wood morphology varied among plants (whole model F5, 38 = 11.0, P < 0.001, species F2, 38 = 16.9, P < 0.001 – F is variances ratio) and, except for M. setosa, was different in parasitized and healthy plants in all variables measured (F1, 38 = 11.1, P = 0.002). Aside from vessel frequency, M. setosa did not respond to parasitism in the other variables we measured (Fig. 19). Also, the effect of parasitism depended upon the plant species (interaction species × parasitism F2, 38 = 7.1, P = 0.002, Fig. 19). Fiber and vessel element lengths and tangential diameter tended to be greater in healthy plants (but not in M. setosa) while vessel frequency tended to be less than that in parasitized plants (in all three species, Fig. 19). Interactions may be due to correlations between vessel frequency and tangential diameter (r = -0.56, P < 0.001) and between tangential diameter and vessel element length (r = 0.37, P = 0.01). One should think that this result is only the influence of diameter, as the thinner trunk is also a response to parasitism, but no correlation to trunk diameter was found.

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800 Parasitized 100 Healthy 700 80 70

600 60

50 500 40

400 30

Fiber length (µm) 400 Tangential diameter (µm) Tangential 40

-2 30 300 20

10 200 Vessel Vessel frequency mm Vessel Vessel element length (µm)

M. foliolosa M. maguirei M. setosa M. foliolosa M. maguirei M. setosa Figure 19: Comparisons of morphological characteristics of parasitized and healthy plants (MANOVA), based on analysis of log-transformed measurements and showing reverse trans- formed averages and 95% confidence intervals. Note that the Y axis is log based.

DISCUSSION

The results showed clearly that the presence of the parasitic plant Pilostyles ulei is re- lated to reduction in host size and changes in wood anatomy. Even without experimental tests for physiological responses, we may hypothesize some plausible explanations for these responses, based on the extensive literature available on the relationships of structure and function of wood. Traditionally, parasitism is thought to have a cost for the host (Price 1977) due to some resource that the parasite diverts from that host. Here, with the parasite Pilostyles ulei and three species of Mimosa, we suggest that the most limiting resources may be water and sugar. Recent evidence demonstrates that these two factors are closely re- lated (Escher et al. 2004). On the one hand water deficit can influence a variety of processes and structures as- sociated with plant growth, with cell expansion being one of the most sensitive (Hsiao et al. 1976; Bradford & Hsiao 1982; Tyree & Jarvis 1982). Thus we hypothesize that, here, the parasite diverts water from the host plant and this is the cause of the changes

Downloaded from Brill.com09/30/2021 04:29:34PM via free access 10 IAWA Journal, Vol. 32 (1), 2011 in the host plants. In the cambium, specifically, water deficit interferes with cell expan- sion, thickening and differentiation (Kozlowski 1971; Fritts 1976), due to the influ- ence of water shortage on metabolism in the cell wall (Whitmore & Zahner 1967). In the cambium, cellular expansion is inhibited with water deficit (Doley & Leyton 1968). The parasite may also interfere with total evapotranspiration of the host. For example, when flowers break through and compromise the epidermis, cortex and peridermis, water loss may follow, because blossoming and fruit /seed maturation last for many months. Indeed, structural changes due to parasitism described here are similar to those found in studies of hydraulic stress in plants. For example, shorter fibers and vessel elements in parasitized plants, along with the inverse correlation between tangential vessel diameter and vessel frequency, are often found in plants from arid regions (Baas et al. 2004; Carlquist 1977; Barajas-Morales 1985) and plants stressed in other ways (Baas et al. 1984 and several other papers). One might expect the host to develop wider vessels to overcome the water loss as- sociated with parasitism to greatly increase water conduction (Baas 1982; Zimmermann 1983; Carlquist 1988). However, wider vessels may be too vulnerable to cavitation, which will reduce conductivity (Zimmermann 1982, 1983). In the case of P. ulei, its sinkers penetrate the xylem, disorganizing and wrapping around some vessels (mostly shorter vessel elements as they are diverted more easily. Thus, when parasitized, ves- sels are often smaller and the total hydraulic conductivity probably is reduced. Mimosa setosa only seemed to respond to parasitism in vessel frequency. This species is found on soils that typically have more water than the substrate of the other species. Thus, perhaps this species was less water-stressed due to abundant water, thereby avoiding the same reactions of the other two species. In M. maguirei the relation of more vessels associated with smaller vessel diameters in parasitized plants was stronger than that of M. foliolosa, yet both are found in similar habitats in the Serra do Cipó. Thus, when parasitized, wood anatomy seems to adopt a more xeromorphic profile. On the other hand, it is well documented that parasitic plants can cause effects on plant growth and allometry (Press & Phoenix 2005; Heide-Jørgensen 2008 and refer- ences therein); we also hypothesize that the reduction in size of parasitized plants is influenced by a reduction in sugar availability. Blossoming and fruiting are some of the most important energy drains in the plant life cycle as has been demonstrated in classical papers (Murneek 1932; Wardlaw 1990). This drain occurs normally when the host blossoms, but parasitized plants, in addition to investing products of photosyn- thesis in its own growth, also lose them to the parasites (Press 1995; García-Franco et al. 2007). Parasites, during reproduction, produce many flowers and fruits along the stems of the host, and these flowers may produce copious quantities of nectar and store sugar, starch and oil in fruits and seeds. Thus, parasite flowering and fruiting are quite probably important drains on host plant resources thereby limiting the ability of the host to grow and reproduce. This also is suggested in M. setosa as we noted that parasit- ized plants, while anatomically changing very little, were smaller than healthy plants. These findings are also in agreement with those found by Gomes and Fernandes (1994) who showed that the direct reduction in plant size due to parasitism of Pilostyles ulei

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(P. ingae) can influenceM. maguirei architecture through reduction in apical dominance and consequent increased branching. Probably this also increases water loss through transpiration due to greater surface area as suggested in the case of Bdallophyton (García-Franco et al. 2007). This form/size effect might be the ultimate expression of the action of the two limiting factors: water and sugar. Many dark cells with phenolic substances were found in parasitized plants. We inter- pret this as evidence of plant defense, similar to that used to defend against herbivores, fungi, viruses or galls. In conclusion, the endoparasite Pilostyles ulei presence provokes changes in the vascular organization and size reduction in the host plants. These anatomical modifica- tions are similar to other stress responses and might increase the safety of the vascular system, by increasing vessel frequency and reducing their diameter. Yet, each species responds somewhat differently to the endoparasite. The consequences of these differ- ent reactions for future reproductive success of the plants should be studied to better understand the importance of endoparasitism.

ACKNOWLEDGEMENTS

We thank Antonio C.F. Barbosa of the Instituto de Pesquisas Tecnológicas do Estado de São Paulo and Gisele Costa of the plant anatomy laboratory of the University of São Paulo. Thanks also to Dr. Veronica Angyalossy from University of São Paulo, to colleagues of University of São Paulo for help in the field and stastistical analysis, Adriana Costa, Bruno Balboni, Giuliano Locosselli and Viviane Jono; and to Celso Lago from IBAMA for providing field facilities. This work was supported by the Research Support Foundation of São Paulo State - FAPESP (Procs. 05/55172-4, 03/10277-8) and by the Brazilian Council for Superior Education - CAPES. James J. Roper translated this manuscript from the original Portuguese, and provided constructive criticism for the text and analyses.

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